Graham Hoyle (1984).



Graham Hoyle (1984).
T H E B E H A V I O R A L A N D B R A I N S C I E N C E S ( 1 9 8 4 ) 7, 367-412
Printed in the United States of America
The scope of neuroethology
Graham Hoyle
Institute of Neuroscience, University of Oregon, Eugene, Oreg. 97403
Abstract: Neuroethology, an interdisciplinary subdivision of neuroscience, has emerged in recent years. Since 1976 there has been a
regular session under this heading at the annual meeting of the Society for Neuroscience. In 1980 two introductory texts in English
were published on the subject (Ewert 1980; Guthrie 1980), and a third (Camhi 1984) was published recently. There is widespread
interest in neural mechanisms underlying behavior, but they encompass such a vast array of often unrelated topics that proponents do
not share common goals. This article describes the emergence of ethology as a discipline, pointing out that its practitioners were
successful because they confined their research to stereotyped, complex, nonlearned, innate behavioral acts. A limited number of
profoundly significant principles emerged. Each of these is redefined. The major concepts of earlier ethology were embodied in a
simple hydraulic model used by Konrad Lorenz in 1949 (Lorenz 1950). It is pointed out that this model implies the existence of
common neurophysiological mechanisms and neuronal circuitry. This model has now been made obsolete by neurophysiological
progress, but with appropriate ~nodificationsan updated version may still be useful in focusing attention on possible principles. The
initial aim of neuroethology should be to examine the neurophysiological events in a variety of behaviors, exhibited by diverse
animals from different phyla, which meet the criteria of innate behavioral acts. The behaviors should be sufficiently complex to
interest ethologists, yet they should be addressable with neurophysiological methods down to the cellular level. In the case of
vertebrates this may mean working with brain slices as well as whole animals, but for some invertebrates recording should be possible
in the nearly intact animal duringexecution ofthe behavior. The work will be exacting and very difficult, and it is not likely toget done
at all unless neuroethologists recognize that they should both train and discipline themselves and restrict their attention to welldefined goals.
Keywords: behavioral biology; behavior patterns; ethology; fixed action patterns (FAPs);instinct; learning; Lorcnz; lnotor programs;
Historical origins of ethology
A scientific discipline of neuroethology could not have
existed either before the term "ethology" had become
established o r before neuroscience had developed to the
point where both neuroanatomical and neurophysiological methods were available that could b e used to attack
ethological questions. There is a strong tendency to
. equate neuroethology with the neural bases of behavior
in the broadest sense. T o d o so encompasses such a broad
spectrum of phenomena that the extremes are virtually
unrelated and can only b e linked by the widest stretches
of imagination. Such links are too tenuous. If the term
"neuroethology" is to serve the useful purpose of identifying a group of active scholar-investigators sharing common goals, to bring them together and stimulate their
research, it must be relatively narrowly defined. There
are clearly dangers in defining any subject too narrowly,
because this can lead to t h e arbitrary exclusion from
serious consideration ofinformation, especially of that yet
to be discovered, that is truly relevant and significant for
t h e mainstream. But the danger is much less than that
associated with using a definition that is too broad. Unless
the focus is restricted, the subject matter expands into a
diffuse vapor without any substance a t all.
The first potential trap is to assume that the term is
merely a faddish one, culled to draw attention to a
previously nameless b u t ancient line of inquiry. T h e first
6 1984 Cambridae Univenitv Press
experimental investigations into the possible functional
relations of a nervous system t o behavior were undoubtedly those of Galen made 1,800 years ago. There is a
direct line from his unparalleled starts, through the ideas
of Descartes and the experiments of Francis Glisson and
Albrecht Haller, via Charles Bell a n d Francois Magendie, to those of Johannes Miiller and his pupil Emil du
Bois-Reymond, who can be considered to have founded
modern experimental neuroscience. Spice t h e above
with some Galvani, Hall, Helmholtz, Weber and Bernstein; then mix with some Gall (no pun intended),
Fechner, Wundt and Titchener, and finally, a liberal dash
of Pavlov and Sherrington, bake, cool, then top offwith an
icing of Cajal and Golgi, and you have neuroscience cake.
The point is that here we have the product of the
combined histories of much of physiology, medical neuroanatomy, and psychophysics. But still this was not
nearly enough to provide a satisfactory basis for the
understanding of behavior, although in many circles,
especially Russian and British ones, it was considered
more than adequate. Even a generation of American
pioneers in the study of behavior, Whitman (1819), Craig
(1918), McDougall (1923), Russell (1934) and eventually
B. F. Skinner [see special issue on the work of B. F.
Skinner, BBS 7(4) 19841, had failed t o realize that something important had been left out. Fortunately, careful
and systematic examination of examples of the behavior,
in natural rather than laboratory settings, of a variety of
Hoyle: Neuroethology
animal species, especially of relatively lowly forms including invertebrates (though mainly insects), enabled a
group of Middle-European zoologists to detect some very
important missing ingredients in the mixture.
For the animal kingdom as a whole, the majority of
even the most complex behaviors, the ones with the
longest sequences of coordinated movements and the
subtlest interactions with other individuals of the same
species, fall into the category of instinctive acts. They
require no experience of the behavior in its context, nor
learning, for their perfect execution. Such behavioral
sequences can be broken down into a few discrete coinponents. each a distinct act or subroutine. Some of the acts
could be recognized as also being performed by related,
but different, species in which they occurred in a different sequence. In a few instances it has been possible to
show that Mendelian laws apply to the inheritance of the
ability to perform these acts.
The realization that there is genetic involvement with
chunks of behavior provided a major breakthrough in the
understanding of how complex behaviors have evolved.
Natural selection clearly acts on the totality of the behavior. But at some evolutionary stage, what eventually
became a subroutine must have been a complete behavior. Possiblv an entire subroutine can a ~ ~ easa ar mutation and become incorporated in a sequk;lce if it confers
selective advantage. But in spite of the simplicity and
fundamental importance of these findings, they sank into
the minds of a majority of both behavioral scientists and
physiologists very slowly. In fact, it was not until the 1973
Nobel Prize for physiology or medicine was awarded to
Konrad Lorenz, Niko Tinbergen, and Karl von Frisch for
their pioneering studies in these aspects of behavior that
the majority of psychologists and biologists interested in
behavior even accorded the work any attention. When
the news broke in the United States, it did not receive the
, laudi its associated with Nobel ~ r i z eannouncements in most of the relevant quarters. Quite the
contrary! While the furor.was still raging, students of
animal behavior were crowding libraries trying to find out
what these "unknowns" had discovered; indeed - what
was the fuss all about? Details may be found in a fascinating historical account by Thorpe (1979).
Lorenz, who was Tinbergen's source of inspiration, and
who was clearly the first person to understand the significance of what the Middle-Euro~eannaturalists were
discovering, frequently used the term Ethologie to designate the subject of his interest. He first used it in the title
of a 1931 paper, published when he was 27 years old, on
the behavior of crows (the uniquely European one he
worked with is called a jackdaw). The term "ethology"
had been around in various contexts for more than half a
century before Lorenz used it. Wheeler (1902)had used it
in a context somewhat similar to that of Lorenz. but it was
still confused with purely descriptive natural history
observations and even with ecology. Clearly Lorenz did
not start out making penetrating generalizations: Indeed,
his avowed first love was studying the natural history of
birds, simply because he enjoyed watching them and was
curious about their behavior. Such was the unlikely path
which led to intellectual distinction and the ultimate in
scientific recognition. It was Niko Tinbergen, however,
who was responsible for the successful publicizing of
ethology. The subject came to be well known shortly after
his book was published in 1951. He referred to The Study
of Instinct as a "programme for ethology" in spite of the
The word "instinct" is derived from the Latin instinctus, past participle of instinguere. The origin of this
word was associated with the use ofa pointed stick, and it
can mean "to prick." Instinctus, as used by Cicero, is to
be incited, or fired up - doubtless equivalent to the
responses engendered by being jabbed. This is very
clearly a reflex action. Paradoxically, that is not what
Lorenz wanted to convey. The whole "point" of the
ethological movement was that it uncovered a multitude
of common behaviors that are not akin to reflexes. even
when triggering is involved. To emphasize the difference
ethologists sometimes referred to the behavior as "endogenous" - generated from within. A reflex will occur at
all times unless it is either habituated o r centrallv SUDpressed during the execution of other behavior. An instinctive behavior will occur only when there is a central
nervous system readiness. Lorenz termed this the "action specific energy" for that particular behavior. Thorpe
(1979) and others have done ethology a disservice by
erroneously attributing to Lorenz the designation "reaction specific energy," which connotes reflex action.
Lorenz thought in terms of a gradual accumulation of a
"reservoir ofuenergy" for the bLhavior in question, which
must be full, or nearly so, or the behavior will not occur at
all. But no catchy word or phrase has yet been coined that
adequately conveys the endogenous aspect. Since the
success of the Lorenz-Tinbergen studies, the term
instinct has come to be used differently from the way it
was formerly, and it now carries with it the implication of
at least partially endogenous generation. he aspect of
releasability and the implication of spontaneous appearance were, even in Roman times, associated with the
word instinctus. Those were times when emperors, in
~articular.used to "flv off the handle."
In Germany, there had been a move toward a scienceof
neuroethology in Erich von Holst's Max Planck laboratory of Verhaltensphysiologie (founded at Seewiesen,
where Lorenz already had an Abteilung); this laboratory
nurtured cybernetics pioneer Horst ~ittlestaedt.But this
movement was content to treat the nervous svstem as a
"black box." It was successful in uncovering some new
principles about nervous system function, the most
important being that for a short time a memory of motor
output, the efference copy, is established and heeded.
The prevalence and importance of feedback, especially
the reafference, was also emphasized. But in spite of the
functional importance of the efference copy, we still have
no direct knowledge of its nature more than 30 years
later. There was a marked lack of interest in direct
neuroanatomicallneurophysiological investigation. Unfortunately, this line of progress was finally stilled when
von Holst became preoccupied with improving the
sounds produced by asymmetrical violas. Fortunately,
this situation is being rectified, particularly within the last
few years and especially by Lorenz's successor at
Seewiesen, Franz Huber, and by Ulrich Bassler, Norbert
Elsner, and Gernot Wendler.
I first began to think of the possibility of a science of
neuroethology in 1951, when I was learning about and
beginning to practice neurophysiology, and after I had
experienced the impact of the LorenzianITinbergenian
Hoyle: Neuroethology
concepts. The research question I was asking was a
specific, simple one, suggested to me as a thesis project
by Bernard Katz, "How can a phytophagous insect produce nerve i m ~ u l s e swhen its blood contains large
amounts ofpotassium and very little sodium?" The insect
I worked on was the locust, and I spent a lot of time simply
observing the insect's behavior. My friend and colleague
at the time, Peggy Ellis, was intensively studying the
marching behavior of nymphal locusts. She had discovered how to induce them to march routinely under
laboratory conditions. Marching is the form of field behavior shown by immature (flightless) locusts, in place of
swarming. Huge bands of immature locusts walk together, as do naturally wingless species as adults. This
behavior has some aspects of the kind of stereotyped
behavior. termed a "fixed action pattern" [FAP), which
was the cornerstone of the ethology movement.
In marching both the posture adopted and the style of
locomotion are different from those of ordinary walking.
S~ecialconditions, a fair amount of e l a ~ s e dtime, a
minimum number of animals per unit space, and the
absence of food are required before marching will commence, but given these circumstances, it is quite certain
that marching will occur. Once it is well under way, the
accessibility of food will not stop it; the insects simply pass
over and ignore the food until they are exhausted. Then
and eat voraciouslv.
, sto~
My physiological work showed that the neuromuscular
junctions, but not the nerves, which are protected by a
regulatory sheath, would be affected by the ionic comDosition of the blood. Therefore. ifa FAP were initiated in
locust in the manner implied by the Lorenz model, the
expression of the output would be affected by the blood
ion concentrations. Theoretically, the range would be
from no behavior at all, through feeble mimicking, with
poor posture, to supranormal intensity, depending on the
potassium, which is high after feeding. Peggy Ellis and I
tested this hypothesis experimentally (Ellis & Hoyle
1954; Hoyle 1954), with affirmative results: Locusts that
have recently fed do not, and cannot, march. Starved
ones march the most vigorously. John Pringle (1939) had
shown for the cockroach, and I confirmed for the locust,
that the innervation of insect muscles is extremely simple, some muscles of functional importance in behavior
receiving but a single excitatory axon. Therefore, the
neural output is easily recordable and quantifiable. That
realization was for me the beginning ofa neuroethological
approach. This may not have been considered to be a new
field of inquiry, but it certainly felt like one. I know of no
precedent for the experiments I did with Peggy Ellis, or
for our interpretation, which was backed by a film shown
to the Society for Experimental Biology.
The principle of a dependence of behavioral expression
on peripheral as well as central factors should apply to
other animals, including man. That this is true is amply
evident in the behavior of persons suffering from episodic
hyper- and hypokalemias. Cornplete motor paralysis occurs in humans, as it does in locusts, when blood potassium levels are at their highest (Creuzfeldt, Abbott,
Fowler & Pearson 1963).
Peripheral neuromuscular events, which are easily and
precisely understood, turned out to be key ones in locusts
and humans, and it was important to have drawn attention to the ability of altered peripheral transmission to
play a role in determining behavior. To my knowledge,
this was a possibility that had not previously been considered, and for me it derived directly from the Lorenz
model. Now. how to ~ r o c e e dto work out the CNS
(central nervous system) events? Sherrington (1906) advanced knowledge of central nervous mechanisms indirectly by studying movements. Words to the effect that
"movements provide us with a window into the nervous
system" indicate the principle that guided him. I decided
to adopt this principle for use with arthropods (see Hoyle
1970). It proved possible to record from several different
muscles of insects at the same time, during several kinds
of behavior, including courtship songs ouf crickets and
grasshoppers, and associated movement sequences.
These turned out to be perfect examples of FAPs. The
study in turn helped to define the FAP concept. This line
of work has since been developed by many investigators
to the state of a fine art, especially by Norbert Elsner in
Germany (see Elsner & Popov 1978). The myograms
provide a simple, quantitative measure of precisely what
the nervous system puts out in order to cause the behavior. From the data a great deal can be inferred about the
nervous system strategies involved in determining particular behaviors. Such data are of value in comparing
related species (Elsner & Popov 1978; Ewing & Manning
1966; Lindberg & Elsner 1977), and in studying genetic
aspects ofbehavior control (Bentley 1971; Bentley & Hoy
1972; Hoy & Paul 1973). There are some behaviors of
some organisms, notably some nudibranch molluscs, in
which the discharge of some identified interneurons is
obligatorily and precisely reflected in the execution of a
particular movement. Myographic data can in such cases
be dispensed with in neuroethological analysis, but for
arthropods and vertebrates, which have articulated skeletons. and which therefore use a balance between forces
in codperating agonists with those in cooperating antagonists, myograms are essential. This is because exactly
similar movements are produced, at different times, by
widely different, detailed motor patterns. In order to
understand the rules underlying control, it is necessary to
know these details and how they relate to the movements. In such cases the CNS must either be using
proprioceptive input extensively or making very sophisticated calculations of the movements that should result
from various combinations of motor output (see Selverston 1980).
These requirements place constraints on the level of
analysis that is possible for any given system. There are so
manv motor neurons active when anv vertebrate makes a
movement that precise, comprehensive myography is
impossible. Only in arthropods is precision possible, and
then only for those muscles that have, or use in a given
movement, no more than four excitatory axons per muscle (though with computer analysis it is possible to increase this limit).
The next-higher step concerns the premotor interneurons. Prior to the introduction of intracellular dves in
1968, studies of this stage were restricted to guesswork
except with a few molluscs that had unusually large,
pigmented neurons. The latter organisms are mostly
aauatic and lack limbs. Their "behavior" is restricted to
the bending of their soft. unarticulated bodies in water, so
it is necessarily less complex, with fewer adaptive variants, than that of terrestrial animals locomoting on legs.
Hoyle: Neuroethology
This is not to say they have nothing to contribute to
neuroethology. The only demonstration that any CNS
can produce a FAP in the absence of inputs other than a
trigger (or releaser) has come from one of them, the
nudibranch Tritonia (Dorsett, Willows & Hoyle 1973).
Much ofour knowledge of basic cellular neuronal properties has been derived from Aplysia. The technical advantages offered by the giant neurons of the abdominal
ganglion have led to an extensive exploration of the
limited movements controlled by this ganglion (Kandel
1976; 1979). But the reflex movements studied by Aplysiologists unfortunately do not represent the kind of
behavior that constitutes the science of ethology.
Future research needs to combine the study of behaviors that have been of sufficient complexity to excite the
serious interest of the giant pioneers of ethology with
analysis of the neuronal circuitry underlying those behauiors. This is a tall order, but thanks to intensive efforts
during the seventies and continuing today, the circuitry
underlying one modest FAP, the leap of the grasshopper,
has now been worked out. There may be neurons other
than those currently known to be involved in the jump,
but they are unlikely to be playing more than minor roles.
A circuit diagram of the neurons is shown in Figure 1. The
behavioral features of a jump have been described
(Heitler 1974). The jump can be elicited by many different modalities of stimuli. A brief change in anv of a wide
range of external factors, such as movement in the visual
field, light intensity, temperature, sound, air puff, touch,
or chemical stimuli, can cause a jump. The insect will also
jump spontaneously, meeting the vacuum-activity requirement for qualification as a FAP; unevoked jumps are
likely to occur in conflict situations, for example, when a
competing male appears during a courtship approach.
This behavior may be analogous to what has been called
displacement activity in vertebrates. It should be borne
in mind that a jump is not simply a reflex response. Either
flexion or fast extension of a single hind leg tibia occurs as
reflex responses to appropriate stimuli but results in
either kicks or preparation for jumps only. There is no
known condition under which a jump is bound to occur:
At times grasshoppers will fry to death on a hot plate,
suffer death by crushing, or be eaten rather than jump.
We do not vet know what the central factors are that
determine the readiness to jump, but there is increasing
knowledge about modulatory neurons that seem likely to
be involved, and answers to the question should soon be
forthcoming. Although it is certainly possible that a
grasshopper's brain can "command" the insect to jump
(or not jump), such a command is certainly not necessary
for a jump. The neural machinery necessary and sufficient
for a jump resides within the third thoracic ganglion
alone. Lateral, ascending, and descending inputs converge on this circuitry and may, individually or cooperatively, set it into motion. [See also Kupfermann &
Weiss: "The Command Neuron Concept" BBS l(1)
It ;ay be argued that the parallel development of
interest in various aspects of neuroscience, from developmental (e.g., Coghill 1929) to cellular, in the 1920s,
1930s, and 1940s simply merged with ethology, so that at
no stage was there a conscious emergence of neuroethology. As it happens, we can easily see that this is
incorrect. At the same Cambridge meeting in 1949 at
II 1
coc kea
Figure 1. Diagram of specific identified neuron circuitry involved in the locust/grasshopperjump. This is a simple, unitary
fixed action pattern (FAP)of behavior. Several laboratories have
contributed details. The neurons are as follows:
1. Motor neurons. Fast extensor tibiae (FETi - Hoyle 1953).
Three sets of flexor tibiae (F1 - Burrows & Hoyle 1973).
2. Interneurons:
Visual. Lobular giant movement detector (LGMD - O'Shea
& Williams 1974). Descending contralateral movement detec-
tor (DCMD - Rowell 1971).
Vibrationlsound. Giant interneuron sensitive to both vibration and sound with a cell body in the mesothoracic ganglion,
traveling from the metathoracic ganglion up to the brain (G Rehbein 1976). '
Multimodal. (a) Supplier of coactivation to flexors and extensor tibiae (C - Pearson & Robertson 1981). (b) Supplier of
excitation to the extensor but inhibition to the flexor, the last
link in the chain, the jump-trigger interneuron (M - Pearson,
Heitler & Steeves 1980).
3. Modulatory neuron. Oveiall humoral-typeexcitatory modulation, both centraI and peripheral, is provided by a dorsal,
unpaired median neuron innervating both regions of neuropil in
the ganglion and the extensor muscle (DUMETi- Hoyle 1974).
The substance synthesized and released is the phenolaminc
equivalent of norepinephrine, octopainine.
which Lorenz presented a hydraulic model (to be described below), the collected views of the traditionalists
were summarized by Paul Weiss (1950). Weiss produced
a rather vague diagram (Figure 2) full of cross-connecting
arrows linking component "centers" for the generation of
complex behavior. There are levels, from inputs to outputs, in terms of specific motor neurons. The most significant aspect, which certainly was universally accepted at
the time, was that there was a strict hierarchy, with tiers
of control systems. The diagram is also notable for its
open-loop character: There were no feedback elements
anywhere in the system. It should be recalled, however,
that this was only one year after the publication of
Norbert Wiener's Cybernetics (1948), in which he took
physiologists to task for not understanding the signifi-
Hoyle: Neuroethology
Figure 2. Early hierarchical concept of control of behaviors of
a typical quadrupedal vertebrate (from Wciss 1950).
cance of the control systems they had discovered to be
widespread in all forms of animals. The ethologists were
as naive about the neurophysiological significance oftheir
findings as the neurophysiologists were about the behavioral implications of theirs.
When stripped of the vast foliage of observations on
individual behavioral acts of a wide variety of species, the
core ofstrictly ethological knowledge boils down to a very
few, profoundly simple, statements. The ethology pioneers left a legacy of novel classificatory terms, each of
which conjures up a clear image of the relevant behaviors.
Within each category, examples of these behaviors are
found in men, other mammals, birds, reptiles, amphibians, fish, insects, crustaceans, some molluscs, some flatworms, A d even some sea anemones, thereby encompassing all levels of neuronal organization yet evolved.
Therein lies the profundity of the findings. These terms
are presented below, with simple, widely accepted definitions, and remarks relative to the discussion that
Definitions of key concepts
1. Fixed action pattern (FAP). This is a complex, coordi-
nated movement or secluence of lnovements that recurs
in a similar manner whenever it is performed. There is a
beginning, a middle, and an end for a sequence, and the
components occur only in one order. A se q uence never
begins in the middle. The act as a whole has adaptive
significance. It is generally performed only in a specific,
biologically significant context. At a given temperature
the time-relations ofcomponents are very nearly constant
whenever the FAP occurs. Only minor variations occur in
response to external stimuli applied during the movement. Most or all of the com~onentsof a FAP are
expressions of inherited factors and are subject to the
Mendelian laws of inheritance as wholes. Examples are
escaDe swimming in some sea anemones and alsoin some
molfuscs, nest-building in some insects, fish, .and birds,
courtship and sexual behavior in some molluscs and many
arthropods, facial expressions in primates, and a wide
range of territorial, aggressive, defensive, and sex-related
acts in all vertebrate orders.
FAPs, are elicited only by highly specific situations or
stimuli (releasers), except on rare occasions when they
may occur spontaneously or in an inappropriate, stressful
situation. The recognition and specification of FAPS has
been by far the most important outcome of the work of
There are also numerous examples of behaviors that in
most respects resemble FAPs, but in which a part, parts,
or the whole are not always performed with equal vigor.
They may have reduced excursion amplitude, reduced
force, less speed, or fewer cycles of repetition. Several
examples are described by Tinbergen (1951), and the
matter has been specifically addressed by Schleidt (1974).
Should these behaviors be given a different designation?
Most ethologists say not, thinking the adjective "fixed" as
best applied rather loosely. Some of these behaviors are
compounded of FAPs and interspersed reflex actions or of
learned actions with or without reflex components. In
such cases it is better to consider the entire behavioral act
as a complex that includes FAP components rather than
to weaken the basic concept, which otherwise has a
precise meaning. If the entire sequence is stereotyped
but has components that vary a great deal in amplitude or
frequency, it is still possible that it should be considered a
FAP. Only a detailed study of the causes of the variations
could decide the true nature of the control mechanisms.
The waggle dance of the bee is a FAP that is modified
quantitatively in relation to the messages to be conveyed:
directions, distance, and quality of food (von Frisch
1967). However, this behavior is clearly a FAP, not a
reflex. Purposive modulation of a FAP for informationtransfer is a very different matter from variation in the
vigor with which a male robin attacks different models of a
male robin.
2. Displacement act. This term is a corollary of the FAP
concept and applies to a fixed action pattern when it is
performed in a context that is definitely inappropriate.
This commonly occurs when for some reason a more
appropriate FAP cannot be expressed, or when the situation is marginal for each of two different behaviors, or
deserves the connotation "stressful." It is often difficult to
make a satisfactory assessment of appropriateness or
otherwise, and mistakes have been made. The important
aspect is that a situation that might release a FAP is often
one that causes widespread general arousal, payingattention, and the like so that one or another FAP is likely to
occur. If the cues are those appropriate to more than one
FAP, especially FAPs that are fundamentally opposite,
such as attacklwithdraw, displacement acts are especially
likely to occur.
3. Releaser. A key concept of ethology, a releaser may be
defined as a specific single organismic or environmental
feature, complex of features, or context, or a behavioral
act or sequence of behavioral acts, performed either by
another individual or by a group of animals, that elicits a
FAP. Releasers range from a simple sign, such as the red
spot on the lower mandible of a herring gull, to an entire
complex sequence of combined auditory and visual
The fact that so many of the behaviors that have been
studied in the name of ethology require a releaser has
been the basis of the more cogent criticisms ofethological
theory, because the releaser + FAP relation appears to
resemble classical reflex action (e.g., Kennedy 1954;
Hoyle: Neuroethology
Schneirla 1952). There is no difficulty when, as is often
the case, FAP expression is an all-or-none one. But what
about a stereotyped behavior whose amplitude is directly
proportional to some quality of the releaser such as its size
or color? Such behaviors have greatly occupied the research attention of some prominent ethologists (especially Tinbergen among early ethologists, 1951), who
were proud of the way they quantified the behavior.
Another controversial aspect concerned the presence of
more than one releaser. ~articularlvwhen the releaser
was an object and the reliased behavior directly related
to the releaser. In such a situation the animal generally
makes a choice and "selects" or displays a preference.
This may be for an artificial object such as a pot egg rather
than a real one, because it is bigger or has more spots or
whatever. The artificial object may elicit constant amplitude behaviors, in which case the FAP concept clearly
applies. The situation is moot for all behaviors in which
the amplitude or intensity is proportional to releaser
quality. The answer to the question, Is this a reflex?, for
such behavior may be "yes," but can, in principle, only be
decided on the basis of knowledge of the neurophysiological underpinnings.
4. Vacuum activity. A complex FAP may sometimes be
performed by an animal in spite of the lack ofany external
releaser. Although, in most cases, the possibility of an
invisible internal "prick" cannot be ruled out, the sudden
appearance of complex behavior suggested to Lorenz the
then-new concept of "action specific energy." He chose
to think of the tendency to show a behavior as proportional to an accumulation of its energy; that energy is
confined within restraining boundaries from which it is
increasingly trying to force its way out. Occasionally the
restraint is overcome spontaneously and the pent-up
energy rushes out, causing action that was appropriately
termed "vacuum activity. "
compromises. But however difficult it [nay be for ethologists trying to quantify their data to handle this particular concept, it is easy to understand what is meant in
general. Termination could be due to a running out of the
neural substrate for drive (see below), or an inhibition
based on performance, especially the consummatory act,
or a combination of the two. Each of these possibilities
invokes neurophysiological phenomena that are amenable to analysis in suitable subjects.
6. Drive and mood. I am well aware that both of these
terms seem quaint to modern ethologists and psychologists. In Gallistel's (1980) The Organization of Action,
the index entry for "drive" advises the reader to "see
Motivation." Nevertheless, drive is defined in the glossary; mood, however, is missing from both glossary and
index. Yet there is no point in dwelling on mere semantics: Nobody truly has any difficulty understanding both
terms and translating them into their personal experience
of behavior. The sight and smell of food are not going to
elicit food-related behavior in an animal that has just
finished filline
" its stomach with attractive food. There are
strong fluctuations in the tendency of any measurable
appetitive behavior to be expressed. Therefore, we can
easilv define both drive and mood and attemDt to determine their physiological underpinnings. [See also multiple book review of Gallistel's The Organization ofAction
BBS 4/41
, , 1981.1
Drive is the probability of occurrence of an appetitive
FAP. Drive is weakest immediately following the relevant consummatory act and strongest when the consummatory act has not been carried out for a long time.
Secondary, capricious variations in strength are superimposed, so that even when drive is strong, a releaser may
not elicit the behavior. Mood is aauantitative variation in
expression of a behavior under apparently constant
5. Consummatow act. There is often a terminal element
in a behavioral sequence that is clearly recognizable as
the objective of preceding preliminary behavior. This is
termed the "consummatory act," and it may be defined as
a fixed or relativelv fixed act that follows a FAP. a
sequence of FAPs, a sequence of reflex actions, or mixtures of FAPs and reflexes, and that is followed by quite
different behavior, or none at all. The entire sequence is
clearly at an end after the consummatory act. This may
be, for example, completion of a nest, orgasm following
mating, or feeding following capture of prey. A consummatory act is especially common after behavior to which
the adjective "appetitive" may be applied unequivocally.
It is the logical climax of appetitive behavior.
The expression "consummatory act" may appear somewhat quaint or old-fashioned to most modern ethologists.
For many behaviors there is an entire sequence of movements, or the repetition of a movement, before termination, and a lot of possibility for feedback influences. A
small amount of good-tasting food may be as satisfactory
as a huge quantity ofpoor-tasting stuff in quenching foodseeking behavior. Some birds overbuild their nests while
others underbuild. Is it the sight ofthe nest, the feel of it,
the amount of work done on it, the availability of nestbuilding material, or combinations of all of these that
leads to termination? Even lowly animals seems to make
Lorenz and his model of instinctive behavior
Lorenz made but one brief excursion into the larger
domain of physiology, which was also the occasion of his
introduction to a broader audience than that of his native
land. This was in 1949, when he accepted an invitation to
address the British Society for Experimental Biology at its
Fourth Annual Symposium in Cambridge. The topic was
"Physiological Mechanisms in Animal Behavior." Lorenz
departed from his usual procedure by presenting a model
summarizing ethological findings that he thought would
make them clear to neurophysiologists. The model, the
sole illustration of his article (Lorenz 1950), was presented in a stunningly powerful yet simple diagram (Figure
3).This model quickly became famous, or in some circles
infamous. It is known as the "water" or "toilet"
("hydraulic") model and indeed, actual domestic porcelain objects have been used in dramatic "live" simulations. Lorenz wrote of his model that "it is able to
symbolize a surprising wealth of facts really encountered
in the reactions of animals." H e further iustified it with
the statement, "As an instrument for the iuantification of
external and internal stimulation, this model has proved
to be of some value" (D.
The toilet model has come to symbolize neuroethology
Hoyle: Neuroethology
Figure 3. The famous Lorenz (1950) hydraulic model, illustrating the concepts of the generation of instinctive behavior
developed by ethologists.
whether persons who call themselves neuroethologists
like it or not, so it can serve the purpose of providing us
with a synopsis for the ethology side of our coin. The
model intentionally implied a physiological underpinning
for FAPs and their "release." In the model, behavior is
simulated by water jets, at the lower right. The rigid
sequence of component behaviors of a specific FAP is
indicated by the slope of the trough (Tr.), and the actual
sequence by the numbered scale (G).The central nervous
system gradually builds up drive for execution of this
FAP, symbolized by a trickle ofwater (T) gradually filling
up a tank or reservoir (R) of "action specific energy" for
the behavior. The energy tries to express itself as movement by leaving the tank and entering the.trough, but is
blocked by the spring-loaded valve (V). The spring (S)
symbolizes neural inhibition, and it is also the route for
mood, in the form of variations in its stiffness. Releaser
action fbr the FAP is symbolized by a weight added to the
scale pan (Sp.).
By putting a series of the reservoirs side by side, and
allowing some parallel or "leaky" plumbing, one could
bring displacement acts into the scheme. The traditional
problem of explaining the utilization of the same movements in several different overall complex behaviors is
also incorporated.
Linking the reservoirs also leads to thinking about a
major problem, that of how an appropriate behavior is
"selected" from the repertoire following the completion
of a complex releaser signal, perhaps sharing some sensory components with releasers of different, inappropriate
The delight of the Lorenz model was that one could
immediately think of a large number of behaviors, in
species from the lowliest diploblastic Metazoa to man (as
witness The Naked Ape, by Desmond Morris, 1967) that
could be fitted into the scheme. It provided all the
magical joy of a great generalization: the illusion of comprehensibility. But was it in this case no more than a
poetic mirage? The water in the model is real enough, and
the physiologist, though unable to specify a precise neurophysiological equivalent, could at least envisage some
possible candidates. The output stages in the model were
very easily understood in physiological terms, since each
is a muscular contraction. The releasers were in principle
equally easy to translate. At their simplest they are signs
that are either present or absent. The sign details often
needed multiple-channel sensory coding: shape, size,
color, and the like sometimes being compourided. But
the final step in information processing could be a 1, O
choice - a single bit of information. A translation of
instinctive behavior into basic neurophysiology of cells
loomed as a realizable possibility, at least for the simpler
invertebrate nervous systems. The science of neuroethology cannot fairly be considered to have predated
the Lorenz hydraulic model of 1949. Neuroethology
could thereafter b e conceived of, and its principal purpose stated. Its pursuit could be equated with testing the
model and, if validated, with the elucidation of the neural
eauivalents of the structural and functional features ofthe
Lorenz model.
and o t h m o v r a l l r+tw#
Modulatory .&bar
and "command"
Figure 4. A 1984 hydraulic model ofbehavior generation, with
special reference to targets for budding neuroethologists. Agonists in a movement, which is part ofa FAP, are indicated as Al,
A,, etc., and their reciprocating antagonists as ANl, AN2, etc.
Modulatable forms of tonus (see review by Hoyle, 1983) are
indicated by T. In the simplest form of truly fixed FAPs, direct
motor tape control without involvement of feedback, the stored
information (simulated tape program 1) is first selected, then
turned on, and via a direct pathway (indicated by dotted line)
activates the relevant interneurons (symbolized by regulators
directing water to appropriate effectors). Other, more varied
FAPs, especially those carrying recently learned information (as
in performance of the honeybee dance) involve complex central
integration of inputs by a neural comparator, and subsequent
modification of the "taped" instructions by a neural computer. A
motor program can also be produced by reference to stored
innate sensory tape information, in conjunction with incoming
sensory and motor information.
Hoyle: Neuroethology
I am told by an eminent ethologist that the "flush toilet
model is not taken too seriously anymore." Clearly,
among other omissions, it lacks the multitude of feedback
processes as well as all the modulatory influences that we
now take for granted as being important factors in all
nervous systems. No allowance is made for behaviors that
are not diminished by performance, especially those in
which there is enhancement from the first in a series of
closely spaced FAP repetitions, to the next.
A modified Lorenz model, which substitutes modulation of neural elements of the FAP-generation circuits for
water filling the tank and incorporates secondary modulations via feedback, both proprioceptive and extrinsic, will
do nicely as a modern substitute. In Figure 4 I have
attempted to draw such a model, again using water, partly
to relate to the Lorenz model but also because a flow of
water is so easy to grasp, but adding a valve-controlled,
pressurized basic system, with electronic controls and
memory, such as we now know are built into even the
simpler nervous systems.
Defining modern ethology and neuroethology
The simplest logic demands that neuroethology be the
study of the neural mechanisms underlying the behaviors
that constitute the science of ethology. To determine
what these behaviors are the neuroscientist should first
read at least the major works of professional ethologists. A
survey of the behaviors and the distribution of species
that are addressed in reviews and textbooks, in the name
of ethology, is revealing. For example, in his classical
work, The Study of Instinct, Tinbergen (1951), by my
count, referred to 473 animal species. Their distribution
according to major classes is shown in Table 1. There is a
strong emphasis on insects and birds, which is not surprising, as Tinbergen loved to watch birds and to experiment with insects. However, in the second edition of a
popular introductory text published much later, Manning
(1972), referring to some 225 species, yields almost identical percentages of birds, which take first place easily
with 37%,and insects, with 19%,as runners-up. This was
in spite of the fact that Manning trebled the proportion of
mammals referred to, from a meager 10%in Tinbergen.
Molluscs formed less than 3% of the total in each, and
these were almost entirely cephalopods.
Table 1. Distributions by class of animals referred to in two
books on general principles of ethology, Tinbergen (1951)
and Manning (1972)
Class of animal
Other invertebrates
An in-depth, independent research program has been
undertaken by a neurophysiologist and his coworkers to
describe the behavior of a lowly gastropod mollusc, Aplysia (Kandel 1979), this species being easy to study
neurophysiologically. There is, nevertheless, no sign that
the remarkable successes in the physiological aspects of
this endeavor have won over ethologists~The ethologists
were there first and are in a position to call the tunes. To
reach them, and thereby promote the unquestionably
exciting and important field of neuroethology, it will be
necessary for neurophysiologists to address the same
organisms and behaviors as do ethologists.
Before proceeding with a discussion of specific goals
and strategies, let us pause to consider how modern
ethologists see themselves and define their subject.
Some authors choose to define ethology very broadly.
The broadest definition is that of S. A. Barnett in Modern
Ethology (1981):"the scientific investigation of behavior
by all means and by all kinds of people." Barnett quotes
John Passmore's familiar passage from The Perfectibility
of Man (1970):"To write anything worthwhile is to arouse
opposition, controversy." Let m e beg to disagree with
him. Even though the great "ethologists" defined their
field loosely, it is very clear both from the subject matter
of their research and their view of their findings that they
in practice came to apply a restricted meaning. Barnett
defines almost everything associated with the study of
behavior except the most important thing of all - he fails
to define what he means by the word "behavior" itself!
My dictionaries offer a variety of choices, of which the
simplest is "movement." Clearly, Lorenz was not a student of movement. Another definition in Webster is "an
organism's muscular or glandular responses to stimulation," that is, a reflex. The very word made Lorenz and
Tinbergen recoil. The whole point of the ethologists'
findings was that there is more to behavior than reflex
action. and I doubt verv much that the intellectual aspects of gastric secretion ever stirred their minds. The
dictionary does go on to qualify the definition with,
"especially movements that can be observed." There are
several scientists who are intensively studying ganglia
such as the one that controls the internal mincing of food
by lobster stomachs, which they regard as a model for the
generation of behavior (e.g., Selverston, Russell, Miller
& King 1976). I concede that what these investigators are
discovering may provide valuable basic information about
the ways in which neurons can be interconnected, and
also abbut the ~
e s enable neural circuits to
* r o* ~ e r t i that
function efficiently. I also concede that this knowledge
may some day serve to guide neuroethologists in some
aspects oftheir studies, but I emphafically deny that such
research is to be considered Dart of neuroethologv.
An ethologist friend who tiinks exceptionally %early
and whose work I admire says that he views ethology as a
"broad concern with what real animals do in real situations." However, close examination of what this ethologist takes the time to study in detail shows that it is
quite restricted: The animals he studies are all furry and
warm-blooded (a fraction of 1%of the animal kingdom),
and only one act of behavior is targeted. It is a major
disadvantage of the field that an in-depth study of even
one behavior can demand the full-time attention of an
investigator plus students. Never has there been a field of
Hoyle: Neuroethology
scientific endeavor where cooperation by experts in different disciplines is more essential.
A program for would-be neuroethologists
We should start by disclaiming the notion that the behavior ofinterest to ethologists is to be equated with any kind
of movement. This route quickly leads to the absurdity of
including in neuroethology a great deal ofphysiology and
biophysics as well as much of neuroscience. The dictionary definitions of behavior also include "manners," "deportment," and "moral conduct." While these again take
us out of the actual realm of the research interests of
Lorenz, they at least introduce the notions ofcomplexity,
of restriction to recognizable clusters, and of interaction
with other behaving entities.
Let us then examine what types of events interested
Lorenz. As we have seen, these were stereotyped sequences of coordinated movements. They were always
ones that were repeated exactly, or very nearly exactly,
not only by any given individual, but by other individuals
of the same species. They were movement clusters
strongly related to survival: escape, defense, attack, territoriality, feeding, courtship/mating, cooperation.
These are all behaviors that relate to the achievement of
goals, and when they occur in man, they are associated
with emotion. They are all classifiable under the term
"instinctive," that is, complex goal-related innate
A careful consideration, and above all, one hopes, a
rational acceptance, ofthese constraints is important ifwe
are to agree upon a working definition of neuroethology
that will promote the development of a useful body of
natural knowledge. Let us enumerate those parts of
physiology that can be ruled out and relegated, as they
always have been in the past, to their appropriate subdivisions of traditional physiology, and along with them the
related neuroanatomy. Neuroethology will doubtless
draw strength and information from some of the rejects,
but should maintain firmlv its "exclusiveness." There will
be many occasions on which a legitimate neuroethological
study overlaps with some of the other disciplines of more
limited scope. For example, I think we should exclude
reflexology, even though some FAP sequences incorporate reflex actions, and also all forms of fundamental and
applied sensory physiology. However, the triggering of
many FAPs depends upon feature extraction, so releasing cannot be fully understood without knowing the
details of this subsidiary action of the sense organs'
Neuroethologists will encounter novel as well as traditional membrane processes down to the level of ion
channels, synaptic transmissions, and electrical and
chemical modulations. Thev will come across familiar.
but also novel, neuronal anatomies and circuits. The
involvement of nonneural cells associated with nervous
systems could become a significant phenomenon for neuroethologists. How, then, will they be distinguishable
from the host of basic physiologists, biophysicists, and
biochemists? Inevitably, neuroethologists wear second,
third, and more hats associated with these disciplines. It
will only be by their assertion of different, more global,
principal goals that they will be recognized. When they
talk to other neuroethologists, all of them will know that
their common purpose is understanding the generation of
particular kinds of complex behavior. There will be a
very few major goals and they will be common. I t should
be possible for neuroethologists to avoid losing sight of
the woods because there are so many interesting trees,
but only if the goals are delimited.
It may be argued that, as knowledge of neuroanatomy
and cellular physiology expands, understanding of the
neural bases of behavior in general, and therefore also of
its subdiscipline, neuroethology, will inevitably achieve
the same objectives, and that this would happen without
any specific focusing on a separate endeavor labeled
neuroethology. I argue against this view. Neuroethology
is quite likely to revert to some earlier dogmas (such as
those of reflexology), or find new ones, if left to the
random pursuits favored by current neuroscience. For, in
neuroscience, we are dealing with a kind of knowledge
that is based on an enormous number of concurrently
interactive, time-dependent variables, in biophysical systems of enormous complexity. The time required to
describe a nervous system adequately is something new
to science. No matter how much effort is expended, it will
take hundreds of years just to work out the elemental
details. Perhaps, as more data accumulate, a general
theoretical framework, which we lack completely at present, will be developed. There is an existing field of
neural modeling that is beginning to expand because of its
potential for practical use in robotics. I expect this to be
highly interactive with neuroethology of the kind I shall
The advantage of defining more limited goals is that a
measure of real understanding at an intellectually satisfying level could probably be achieved within a human
lifetime. There are other potential advantages. The insight ofthe major ethologists I have mentioned prevented
a continuation of the blind following of false leads. A
major outcome of their thought was the realization that
there was more to complex behavior than the compounding of reflexes. The reflex schools of physiology, established by Sherrington and Pavlov, totally dominated both
thinking and experimenting for more than half a century.
Paul Weiss (1941)was thought slightly ridiculous when h e
dared to ask, though in a less-than-global journal, "Is the
sensory influx a constructive agent, instrumental in building up the motor patterns, or is it a regulatory agent,
merely controlling the expression ofautonomous patterns
without contributing to their differentiation?" (p. 592) Sir
James Gray was on much firmer ground in 1949, thanks to
growing understanding of the findings of the Lorenz
school, when he asked the same question in the form:
"Can an animal initiate and maintain patterns of coordinated muscular movement without reference to the outside world?" (Gray 1950, p. 112).
The decline in the dominance of reflexology was not far
away. Major credit for experiments that led to rejection of
a false dogma must go to a very small group of invertebrate neurobiologists, especially the late Donald Wilson
(1972; also see review by Delcomyn, 1980). But the way to
widespread acceptance of their findings had to a large
extent been prepared, albeit unwittingly, by the European ethologists. As we have noted, ethologists mainly
worked on and wrote about birds and insects; they treated
Hoyle: Neuroethology
examples from each class as if they provided equivalent
variations on the common themes of animal behavior.
The general principles expounded were meant to apply
across the board to behaving animals, whether they had a
backbone or not. These ideas about the generation of
many of the behaviors the ethologists studied were clearly incompatible with reflexology, though they did not
make a major issue of this incongruity.
As long as physiologists subscribed to the Sherringtonian1Pavlovian doema that the most coln~lexbehaviors
could, in principle, be understood on the basis of the
compounding of reflex actions, there was hardly any need
for an elaborate, prolonged attack on the question of how
behaviors are generated by investigators armed with
microelectrodes. The relatively recent realization that
many, perhaps most, complex behaviors are generated by
endogenous neuronal activities has completely changed
the requirements. We must now admit that we have no
understanding of the neural mechanisms underlying a
maioritv of behaviors. The onlv wav a behavioral act can
be iul1;understood is in terms ;f t h i actual functioning of
the individual neurons producing the output/commands
and ofthe circuits in which thev
is a verv tall
, o ~ e r a t eThat
order. It is virtually unapproachable for most vertebrate
behaviors: There are far too many cells and they are too
inaccessible to permit obtaining the kind of information
that is needed. This is not to say that we cannot obtain
information of relevance to the central questions from
vertebrates. but that definitive information that will allow
a comprehensive understanding of all but the simplest
movements may be forever beyond our reach.
For some behaviors of some invertebrates there are no
known barriers to eventually obtaining all the knowledge
needed. This is because the relevant neurons are addressable during the execution of the behavior. By combining cellular neuronal knowledge from invertebrates
with whatever can be obtained from vertebrates we
should eventually be able to achieve a satisfactory overall
understanding of the principles underlying the generation and control of behavior by nervous systems. The
closest we have yet come to obtaining complete explanations of FAPs is for a few behaviors of invertebrates from
different phyla. One such behavior is the escape swimming of the nudibranch mollusc Tritonia (Getting 1983;
Willows et al. 1973). This has the singular advantage of
being obtainable in the isolated nervous system, along
with being recordable from the intact animal. The presence of the rest of the animal is not necessary for the
swimming motor neural program to occur; nor does the
rest of the animal influence the production of the program
when it is present. Doubtless many small, specific cellular details remain unknown, but both the triggering (or
releasing) mechanisms and the major details of the patterning are known. Although this FAP is generally elicited by the experimenter with a chemical agent (common
salt), it can occur spontaneously. Another instance of the
study of fictive behavior (i.e., motor output coinparable
to that occurring in the natural condition, but in a semiisolated state) is oviposition digging by female grasshoppers (Thompson 1982). There are some parallels between
the neural mechanisms of digging and of Tritonia swiinming. The locustlgrasshopper jump, whose neural circuit
was referred to above (see Figure l), is different in every
possible way from escape swimming, leading one to
wonder just what the range for arhythmic behaviors is. In
spite of the relatively lowly levels of these behaviors, it is
reasonable to consider these studies neuroethological.
Goals for neuroethologists
Following the lines of thinking outlined above, the primary target for neuroethologists becomes the study of the
cellular events underlying fixed action patterns and related instinctive acts. Although it may seem a trifle redundant, and certainly rather naive, it may be desirable to
spell out precisely which aspects of neuroethology most
need to be tackled. These are:
1. Description of motor neural circuits and the ways
they function in the generation ofa wide range ofcompler
behuuwrs, especially different behaviors using common
2. The precise roles played by proprioceptive, tactile,
and visual feedback in determining behavioral details.
3. The nature and location of the efference cow.
which, one can deduce, plays a major role in determining
motor control of some complex behaviors and in learning
motor skills.
4. Neural events of association between reafference
and the efference copy in behaviors using both.
5. The locations and nature of inherited stores of
information, which can be called upon as "motor tapes" to
produce species-specific behaviors. (Examples are uncapping of cells in a hive containing dead bees and
removing the corpses, two separate behaviors, each of
which is genetically determined and subject to Mendelian laws of inheritance; Rothenbuhler 1964a; 1964b).
6. The locations and nature of inherited stores of
information, which can be called upon as "sensory tapes"
to guide the production of species-specific behaviors.
(Examples are offered by conspecific recognition of song
by insects and by birds, and the "image" of the final
product used in the construction of patterned webs and
nests by spiders, insects, fish, and birds.)
7. Elucidation of the changes occurring in a nervous
system, which determine the progressive change in the
probability that a particular behavior will occur.
8. Determination ofthe neural factors underlying variation in drive for behavior in general and for specific
9. Identification of the neural and associated mechanisms generating circadian and circannual behavioral
10. Determination of neural determinants of changes
in drive following execution of a consummatory act.
11. Analysis of the mechanism of "switching on" of
behaviors by their releasers.
12. Determination of the locations and nature of information stores (memory) acquired by experience that are
used to modulate innate behavior.
13. Determination of the means by which memory
information is utilized in the execution of behaviors.
Hard choices about target animals and behaviors
There has long been a debate in private, and to some
extent in public, about the optimal species/behavior
targets for analysis (e.g., Hoyle 1975; 1976), and the
Hoyle: Neuroethology
question is as far from resolution now as when it was first
raised. Many investigators refuse even to face the question, resorting to bizarre 'j'ustifications" of choices made
for no good reason. I still feel that large insects offer by far
the most promising compromise among interest, significance, and feasibilitv. I confess to feeling somewhat
negative about the eiormous amount of resiarch being
published on Aplysia, though the depth of the work is
exem~larv.Kandel and Schwartz (1982) refer to this
beha;iorally boring glob of squishy p;otopiasm as a "highe r invertebrate." If this is so, the humblest insect must sit
at the rieht hand of God! The research ern~hasison
Aplysia his been dictated solely by the easy accessibility
of its large, naturally colored abdominal ganglion cells. if
some of the immense effort devoted to Avlusia could be
diverted to one or a few truly higher invLrtkbrate(s), we
might see some giant strides in neuroethology. As it is,
there seem to be no principles of integrative or intrinsic
neural functioning that we can extrapolate from Aplysia.
The work is valuable at the cell and membrane level, of
course, but can lead to oversimplifications or can even be
misleading if extrapolated to the behavior of animals with
legs. Cellular descriptions of events in habituation, sensitization, and simple classical conditioning need to be
complemented with information about the cellular mechanisms of the long-lasting forms of learning.
There are such major basic gaps in fundamental neurobioloeical knowledge that some effort to channel efforts
toward resolving them is justified. For example, what is
an efference copy in cellular terms? Where is it located?
Which neurons are addressed when a behavioral "suecies
memory" of a simpler invertebrate is utilized in a fixed
action pattern requiring specific sensory input? Exactly
how do any of several well-known "command" interneurons evoke walking? What really is the "flight motor"
of a flying insect? Where in the nervous system of a bee
are the waggle dance instructions located? One could go
on and on because the list is so long.
The crustacean stomatogastric ganglion and Aplysia
visceral ganglion have been regarded as "model systems." but models of what has not been stated. It is
indeed possible that some neuronal generators of movement cycles in other organisms will be found to work like
the neurons controlling a single locomotor movement of
Aplysia (and like others, such as the stomatogastric ganglion neurons). But these are at best examples ofwhat tnay
be found elsewhere. They cannot be taken as models of
what actually happens in another system until the other
system has been at least partially explored. A model-T
Ford engine is a good model for even the most complex
16-cylinder Ferrari engine, but it cannot tell us anything
about a turbojet. Even a cursorv examination will suffice
to indicate whether or not an unknown engine can be
modeled by the model-T, but the direct inspection must
first be made.
So neurophysiological strategy must involve the exploration of many systems, in addition to. in-depth examination of a few. My judgment is that the choice ofthe ganglia
of Aplysia and the crustacean stomach as targets for so
much attention is not justified on the basis of the significance of the behaviors they generate. The same arguments apply even more cogently to neural circuits controlling hearts, which are also intensively studied, most
recently in the leech by Peterson (1983a; 1983b). Much of
our current knowledge of neural events in relation to
behavior has been obtained from a few insects, notably
locusts and crickets. which are rather limited in reuertoires. However, the brains of bees, whose behavior
certainly commands widespread interest (and respect),
have recently been shown to be amenable to study with
intracellular dye-filled electrodes (Erber 1983). We
should all like to know what goes on in insect brains aside from the processing of visual, chemoreceptor, and
wind sensory information - especially what roles they
may play in generating and controlling behaviors. Bees,
ants, and wasps are guided by species-specific "species
memories" of both individual and group activities. Where
in their nervous systems do they store this information?
How do they utilize it to generate relevant movements?
Until the bee brain has been more intensively examined,
there is still a great deal that we can learn about learning,
using preparations that have proven amenable to cellular
analysis. With insects, we can study operant conditioning
using a paradigm that eliminates many of the experimental objections raised to "learning" the association of two
stimuli, one or even both of which may be aversive
(Forman 1982; Hoyle 1980). The results may be slower in
coming, because the experiments are much harder to
carrv out. but the results should take us bevond such
phenomena as habituation, sensitization, and short-duration associations.
An instinctive behavior of worker bees prompts them
to "recqrd" flight direction and distance and then to use
the stored information for the subtle modulation of an
inherited basic movement pattern. The latter, the waggle
dance, is a good example in the best sense ofa FAP. There
is no difficulty recognizing it, it cannot be confused with
any other behavior of the bee, and it is a set sequence of
movements; however, a few key elements are capable of
variations based upon recent experience. These quantitative modifications are the critical features of the contribution of information: The dance (FAP) is merely a
vehicle for the expression of recently acquired information, by way ofthe variations. The entire question of how
insects acquire any form of new information, store it, and
later use it to modify their behavior is wide open, but it is
certainly amenable to cellular analysis in some species.
Major criticisms of the FAP concept have come from
experiences in which a part of the total expression of a
stereotv~edinstinctive behavior was shown to be clearlv
due to iearned behavior. A particularly clear example is
imprinting, in which the inherited stereotyped behavior
allows for a major element - the object to be followed - to
be learned. There is nothing in the nature of a FAP that
forbids its being altered over the long term by experience, or even by immediate sensory input. Likewise, one
FAP could be followed bv another so~netirnes(but not
routinely) or be mixed with reflex actions.
In addition to their jump, there are other activities of
grasshoppers for which the neural events are at least
partially known, including flying, maneuvering in flight,
the elemental stepping of walking, digginglegg-laying,
and a variety of courtship stridulations. Some of these
behaviors use common motor neurons, yet the motor
neurons appear in each case to be themselves participants
in the circuits. The circuits are complete in headless
animals, so the carrying out of these complex behaviors
does not require input from the head except as a source of
Hoyle: Neuroethology
general excitation. The most significant finding to have
emerged from these cellular and circuitry analyses is that
there is no evidence for hierarchies. Each behavior is the
result of the interactions of a small number of neurons,
which includes some key interneurons located in the
same ganglion as the motor neurons, and the motorneurons themselves. There is no trace of the kind of
hierarchical organization (in the big-business sense) envisaged by Paul Weiss (1950) and others. What the known
nervous system examples actually do is what is done in
modem computing, that is, parallel processing of information. We need theoretical work, combined with modeling, which will enable us to understand parallel
Prospects for neuroethology of vertebrates
I have generally been very pessimistic about the prospects for the neuroethology of vertebrates - and have
often been chided for expressing this view: Presumably,
it all depends what it is that one wants to know. There is
no difficulty in generating data on vertebrates in the name
of neuroethology - quite the contrary. The problem is
whether any of it helps in resolving the major questions
raised above. Even knowledge of neurons and their
circuits is of little value for neuroethology, except in the
context of the behaviors they are associated with. Since I
have called for extensive cell-level knowledge of events
occurring during behaviors as a prerequisite for understanding the neuroethology of invertebrates, how can less
be required for vertebrates? The major retort has been
that invertebrates have relegated significant major functions to single neurons, whereas the equivalent functions
in vertebrates are associated with masses of what are
presumed to be approximately equivalent neurons. Because of the anticipated similarity, it is supposed that
knowledge from any one within a cluster may be transferred to the others. This might be more believable if it
had been demonstrated to be Gue for any given cluster, in
a behavioral context. The possibility oftesting the validity
of the assumption as a principle at least looms a little
larger since the introduction of cellular work on slices of
brains, but the work remains to be carried out. Bullock (in
personal communications) keeps suggesting to me that I
pay attention to the work ofhis laboratory on vertebrates,
which he calls "honorary invertebrates," namely, electric
fish. It is certainly true that weak electric organ discharge
patterns are complex, interactive, and subtle. Furthermore, the motor aspect - generation of the discharge - is
quantifiable, and the sensory return is addressable all the
way into the brain. However, as "behavior" electric organ
activity is highly specialized, does not involve limbs, and
seems remote from the majority of "behaviors" in which
the motor output is expressed as movements.
If we address the relevance of vertebrate studies from
the standpoint of, "It is what neuroethologists who work
on vertebrates do," what comes up? I have two colleagues
who like to be called neuroetholbgists, J. Simmons, who
works exclusively on echolocation in bats (Simmons
1980), mainly behaviorally, and H. Ferllald who studies
features in the visual system of a cichlid fish (1983),
mainly neuroanatomically. Two prominent scientists
working in the United States who like the neuroethology
label are Fernando Nottebohm, of Rockefeller University, and Mark Konishi, of the California Institute of
Technology. The former works exclusively on brain anatomy in relation to the generation of songs by birds
(Nottebohm, Stokes & Leonard 1976), and the latter on
auditory location of prey by owls and the cortical representation of the spatial field (Konishi 1983). Neither is
able to address the motor control questions raised above.
For another source of what is regarded by some as
neuroethology, we can consult the subject matter of
two books on neuroethology, one by Ewert (1980) and
one by Guthrie (1980). Ewert (1980), in the English
translation of his 1976 German text, defines the goal of
neuroethology as relating activity within groups of interconnected nerve cells to behavior. He defines behavior as
"spatially and temporally coordinated patterns of movement" (p. 1). This objective is woolly and, as a dyed-inthe-wool champion of first finding out how invertebrate
nervous systems work, I feel cynically committed to
pointing out that this may be the best that can be hoped
for from studies on vertebrates. (I am mindful of the
demonstration carried out by the late R. C. Gary for his
medical students at the University of Glasgow. He asked
that every student in his class think up a different sensory
input for a cat - any kind of odor, region of touch or pull,
local temperature change, stretch or flexion, movement,
sound, and the rest. Having amassed a long list, he
produced a decerebrate cat with a needle electrode
implanted in its anal sphincter, and started to work
through the list. Every stimulus produced a burst of
spikes!) Featured in Ewert's book, apart from his own
work, are studies on object location by electric fish and
behaviors elicited by local electric stimulation of the
brains of several vertebrates besides toads. The longest
chapter (pp. 71-128) is devoted to "recognition and
localization (in brains) of environmental signals." Ewert's
own research has been on the basic prey-catching behavior of toads, including factors eliciting it and its habituation. He has also examined both the effects of lesions on
the behavior and of focal electrical stimulation, via flexible implanted leads, in toads free to move. These are fine
examples, but of Verhaltensphysiologie rather than neuroethology, at least as I have defined it here.
The author of the other text, D. M. Guthrie, has
worked on invertebrate animals, but h e has devoted
about half of his book to vertebrates. Major topics covered
are Roeder's work (1967; 1975) on bat/moth interrelationships, various visual discrimination(s), association of
regions of brains with sensitivity to specific modulators,
and the production of motor output by mammals.
A cursory inspection of the vertebrate data that are
included in these textbooks, combined with the work
actually being performed by researchers who gladly accept the label of nenroethologist, shows that none of the
data or work arises out of the classical period of MiddleEuropean dominance in ethology. The investigators are
interested, not in behavior in general, but in very highly
specialized aspects peculiar to certain classes. The
favored animals are all specialists: Only song birds sing;
only bats echolate; only electric fish electrolocate; only
owls can hunt in total darkness. There is a surprisingly
strong emphasis on the relevant special sensory input.
Much of classical ethology is concerned with the acts, not
with releaser details. The connections of these investiga-
Hoyle: Neuroethology
tors with each other's research domains are so tenuous as
to be invisible. These investigators are not to be separated from those among their colleagues who are solely
interested in the specific behaviors of the relevant species, and not at all in either neurophysiology or
Recently a large, multi-author volume was published
on Advances in Vertebrate Neuroethology (Ewert, Capranica & Ingle 1983). Although it is true that much of the
work reported has neuroanatomical/neurophysiological
implications, very little of it was directly concerned with
getting at the critical problems of the neural machinery of
behavior. Tinbergen's term Ethophysiology (Tinbergen
1951) much more aptly describes what is in the book than
does neuroethology, in my opinion.
What is needed is focus on both behavioral and neural
circuit functioning. There should be no leaning toward
the principles of neurophysiology, with its reductionism
and intense concern for novel cellular processes. There
should be total commitment to the common themes in the
generation of instinctive behavior listed above. Control of
flow of the water in the Lorenz model is the heart of the
matter of ethology, water that represents basic but still
unknown neurophysiology, neurochemistry, and information flow in neural circuits. These things are knowable,
and their pursuit provides just as big a challenge today as
it did in 1950. The prospects for successful investigations
have been greatly enhanced by the development of new
techniques. The most important of these are the intracellular dyes, which are making it possible to develop
maps of identified neurons, and the use of brain slices,
which has brought vertebrate brains within range of
intracellular electrodes.
Is a general theory of neural circuit function
Unfortunately, in spite ofan explosion of research activity
in neuroscience in the 34 years since the Cambridge
meeting, there has been little advance in its conceptual
underpinnings. The single general framework that has
ever existed, the McCulloch-Pitts (1943) binomial model
of neural function. had to be abandoned when intracellular recording revealed the widespread occurrence
and importance of analog information processing and
signaling (reviewed in Pearson, 1976). But the vacuum
left behind has yet to be filled with even a tentative new
model. Neuroscience came to be the art of the do-able,
with expediency ruling the day, rather than a soundly
based intellectual domain. Three generations of neuroscientists have now been trained without any link to a
widely accepted general theory of neural circuit function
and neural integration. They have been given to believe
that they are engaged in a massive fact-finding operation
guided only by the relative softness of the seams in the
body unknown that happened to face their individual
picks! Science without larger questions provides a dismal
prospect to a truly inquiring mind. Of course, to those
who would make careers out of providing random facts,
nothing could be nicer, so varied and so complex are
nervous systems. There is enough material to occupy
armies of such persons for centuries. But without some
strong delineations neuroscience will continue to explode
into myriad fragments. We shall end u p with masses of
descriptive minutiae of many nervous systems without
advancing our overall understanding of how they do the
iob for which thev evolved.
Although I see no prospect of an all-encompassing
theory, there are some neuroscience clusters for which it
seems possible that theoretical frameworks might b e
devised. First, there is learning, especially the unknown
cellular events associated with memory, its acquisition,
storage, retrieval, and utilization. Second is feature detection by sensory systems. Most anatomy andphysiology
of sensory systems is trivial from the point of view of the
major ethological themes. There is just too much sensory
information available to most animals. and their nervous
systems have been at pains to reduce it to significant
fragments. It is only the extracted key features that
seriously concern behavior.
The third cluster is motor control. There is, happily, a
great deal of common ground in existing approaches to
the general questions of the control of posture and locomotion in all kinds of animals. For historical reasons, this
area has kept sight of the possibility of a theoretical
framework, most recently in tensor theory application
(Ostriker, Pellionisz & Llinas 1982), and ideas have been
usefully adopted reciprocally between students of "higher" and "lower" forms of life. However, this framework is
apparently inadequate. In the 1982 abstract of a Neurosciences Society Workshop on motor control, it is stated
that "Experimentation in this area cannot proceed without theories" and "the uredominant. almost extreme.
empiricism which characterizes research in motor control
might in the long run be disadvantageous for progress"
(Ostriker et al. 1982, p. 155).
The fourth cluster is the most global: information
processing. We know that nervous systems are real-time,
clock-controlled, gated devices, having mixed hardwired circuitrv and ulastic modulabilitv, in which both
digital and analog infbrmation is handled simultaneously
and consecutively. Thinking critically about information
processing in such complex systems should not be left to
aged oscilloscope watchers, accustomed to 10-hour days
making and pushing electrodes. There are professional
theoretical physicists who win Nobel prizes from couches
in rooms furnished only with paper and pencil and a
computer terminal. Neuroscience desperately needs a
comparable coterie. Existing neural modelers are concentrating their efforts on working out computer programs capable of mimicking known cellular events, plus
evaluating quantitatively the effects of changes in the
form of dendritic spines, changes in synaptic conductances. and the like. These mav be necessarv stem. but in
additidn some thinking about,' and modeling of,-circuits,
especially ones with lots offeedback and parallel processing, is long overdue. I have little doubt that, should a
theoretical branch become firmly established and attract
good minds, it would not only benefit neuroscience but
also, in a very short time, completely revolutionize the
science of computing. Of course, laboratory neuroscientists should keep a close watch on these anticipated
theorists to make sure they keep to the facts and propose
valid exueriments.
The filth cluster is development. Spectacular progress
has recently been made in this field by young scientists,
some of whom started out by working in invertebrate
Hoyle: Neuroethology
neuroethology (e.g., Goodman & Spitzer 1979). Goodman is taking advantage of identified neurons discovered by insect neurobiologists, determining when they
appear in the embryo and how they hook up with each
other, and discovering previously unidentified neurons
as a result of following the genesis of neurons. This
information is bound to help in the understanding of
neural circuitry, so this is a bidirectional service. But atits
present stage, discovering the elemental facts of development, this field can properly be left, as it has in the past,
to specialists in developmental biology. Most of the
transferees from neuroethology to neural development
have quickly lost sight of their original goals. They are
now interested in development per se, and molecularlgenetic concomitants. Fine. Let them work out the
details of develo~mentat all levels. When enoueh is
known about any specific nervous system, the details may
well prove valuable to the neuroethologist. But let us,
until much more is known, stop pretending we belong in
the same guild. We all belong to the same city; our
activities interact to some extent, but we each have very
different iobs to do for the time being.
There are other neural matters, too, that can be left to
other kinds of professionals. Kinesis, tropism, and taxis
are in the domain of ex~erimentalzooloeists. Membrane
biophysics has more than enough independent professional adherents. Medically oriented neuroscience produces relevant information but is clearly not of primary
concern. Neuroanatomy I have left out, because it is best
if the relevant anatomy is done, as needed, in combination with the physiological studies, rather than, as has
been the case in the ~ a s.t as
. a seDarate branch of neuroscience. Neuroendocrinology and neuropharmacology
are likewise not valid intellectual subdivisions of neuroethology: They have their own axes to grind.
Qualifications and justifications
Much has been written during the last decade on the
oversimplification implicit in early ethological concepts.
Hardest hit of all has been the very cornerstone of
ethology, the releasable, inheritable FAP, merely because it was found on closer examination that for many
supposed FAPs, the "fixed" aspect is highly suspect
(reviewed by Wolf Schleidt, 1974, and by Barlow, 1977).
Among the most detailed studies are those by John
Fentress and his associates on facial grooming in mice
(Fentress 1980). This is a nice example because it is a
regularly repeated act, and the basic movements occur in
the stumps of mice from which the forelegs have been
removed late in development. The detailed studies
showed that both early and late stages of a grooming
sequence in a normal intact mouse are subject to a lot of
variation. The middle stages are much less variable.
Furthermore, the details ofgrooming behavior are different in mice examined in familiar territory, compared with
similar mice in unfamiliar territory. The imposition of a
load during the grooming may abruptly halt grooming, or
lead to progressive increase in force developed by the
restrained muscles.
It is quite unreasonable to hold the view that such
findings have rendered the "fixed" aspect redundant,
even if it emerges that no instinctive behavior of a
vertebrate is played out in strict conformity with the
open-loop motor tape concept. There are undoubted
instances in invertebrates, notably the escape swimming
sequences of sea anemones and of some molluscs and the
courtship songs of some insects, where no variations or
negligible ones occur. Possibly the ancestral version of
facial grooming in mice was equally fixed. We already
know that there is a full spectrum in the behavioral
repertoires of invertebrates, from ones in which there is
no significant variation in performance under standard
conditions to ones with as much leeway as there is in facial
grooming of mice.
Several people have toyed with the idea of simply
dropping the "F" (fixed) and calling these behaviors
"action patterns." This would be invalid because every
kind of goal-oriented movement is an action pattern. The
original term is well worth keeping as long as the aspects I
discussed above are kept firmly in mind. It is the fixed
aspects of a FAP with variability that are the most significant ones for classification. No amount of variability in a
FAP alters the fundamental fact that, at some time in each
behaving organism's evolution, a genetic change occurred that added a new aspect to the behavioral repertoire for each movement sequence for which we can now
designate a concise descriptive term, such as escape
swimming, courtship song, facial grooming, etc.
There were probably many different routes to any one
ofthese end points in the evolution ofbehavior in terms of
the kinds of neural anatomy and physiology involved.
Furthermore, there may be unique special adaptations
peculiar to one phylum or another. However, these are
not possibilities to be either second-guessed or despaired
of. The very essence of neuroethology should be to
determine, for representative orders of animals from
diverse phyla, precisely what the possibilities are.
In all cases the behavior arose initially as a mutation, or
concurrent set of mutations, which caused novel neuronal
circuitry and connectivity, as well as cell and synaptic
properties and associated modulabilities, to arise during
development. In some cases, these must have occurred in
pathways that already possessed a great deal of variability
due to competing convergent inputs. In others, they will
have affected routes with no other inputs and so led to
fixed actions. The point I wish to emphasize is that,
although the final outcomes will be seen to be markedly
different quantitatively in the variants, the underlying
mechanisms and genetic bases may be found to be
Even now, when we know very little about the neural
generation of FAPs, I would hazard the guess that there is
at least one widespread common feature in the mechanism of their generation in both vertebrates and invertebrates. This feature is the involvement of one or more
interneurons releasing a neuromodulator substance (see
my commentary on the BBS article by Dismukes, 1979,
for definitions) at specific neuropilar sites. I envisage the
appropriate parts of a central nervous system as acting
like a keyboard, which, being struck in certain chord
combinations, produces each specific phrase of a behavior. The same notes in different combinations produce
different phrases. Striking a particular chord is the role of
a specific interneuron (i.e., the command neuron) or
cluster thereof. Where there is cyclical repetition of the
movement, the cycling is likely to be caused by reciprocal
inhibitory relationships of the agonists in the movement
with their antagonists. T h e cycling will continue as long as
the modulator influence persists at a suprathreshold
This hypothesis may b e given t h e tentative label, to
facilitate discussion, of t h e orchestrationlmodulator hypothesis. T h e timing of sequences within the behavior
will depend, in this hypothesis, in part upon the relative
timing of excitation of t h e modulators, and in part upon
the length of time their effects take to become apparent.
This sequence is in no way at odds with the motor tape
concept (Hoyle 1964), b u t rather is a specific proposal as
to the neural substrate of a tape.
It is easy to see, with this model, how variation and
evolution of behavior might come about. Furthermore,
the wide range of "fixity" of a FAP observed is especially
easily understood. T h e mechanism proposed is compatible with t h e known facts of Tritonia escape swimming
(Dorsett e t al. 1973; Getting 1983) and with a recent
discovery in my own laboratory by Sompong Sombati
(1983)that minute amounts of the natural neuromodulator substance octopamine iontophoresed from a micropipette into locust neuropil evoke bouts of specific behavior at very precise locations only.
behavior rather than circuit properties of ner~roche~nistry
se. I also agree that the working out of explicit neural circuits for
insect locomotion (as in Hoyle's Figure 1) is an exciting chapter
in neuroethology. But why must Hoyle exclude much excellent
work that many of us would a c ~ e pas
t enriching neuroethology?
Hoyle defines neuroethology as "the study ofthe neural mcchanisms underlying the behaviors that constitute the science of
ethology," giving an almost mystical primacy to work in the
preneural canon of ethology. Kandel's (1979) illumination of the
cellular mechanisms of learning is dismissed (admittedly in
wickedly amusing rhetoric) because Aplysin does not exhibit
behaviors that interest Hoyle. Ewert's (1980) book on h'euroethology - which includes an exposition of thestudies ofhow a
toad brain recognizes prey and enemy that I have used in my
own work on what I had thought to be (theoretical) neuroethology - is dismissed as Verhnltensphysiologie. Ewert defines the goal of neuroethology as the experimental analysis of
the neural releasing and control mechanisms of behavior.
Hoyle, usingcritcria I find inscrutable, finds this "woolly"- but
it seems to me just as illuminating as his own definition, and all
the better because it does not rely on a prior definition of what
constitutes ethology. Hoyle gives the game away when he
confesses that, while he is not woolly, he is a "dyed-in-the-wool
champion of first finding out how invertebrate nervous systelns
All this is unnecessarily divisive. Let us accept both Hoyle's
and Ewert's definitions as useful approximations; and that some
neuroethologists like molluscs, some prefer insects, but that
many see neuroethology as a path to understanding the human
being, so that many vertebrate systems (spinal mechanisms of
No matter how many o f t h e major themes ofneuroscience
locomotion in cat or visual systems in frog, toad, cat, or monkey)
are removed from t h e specific domain of neuroethology,
become central to their study. Researchers into neural control of
what remains is still a vast spectrum of specialties that
locomotion have learned the value of rich communication becalls for t h e careful assignment of priorities in determintween students ofvertebrate and invertebrate systems. I urge a
ing which need to b e studied most urgently. Regardless of
similarly ecumenical view of neuroethology.
their choice of animal species, neuroethologists might
More theory. I am delighted that Hoyle is a strong advocate of
consider concentrating first on in-depth analyses of the
the development oftheory in neuroethology, but distrcssed that
he has not read any of the literature since "the McCulloch-Pitts
'neural machinery producing FAPs. Once understanding
(1943)binomial [sic] model of neural function." I will offer here a
of the common neuronal events underlying a sufficient
brief selection of entry points to the subsequent literature of
number of FAPs has been obtained, several other major
brain theory, and I will give a number ofreferences to studies on
subdivisions of ethology - elucidation of the neural bases of
vision, learning, and control ofmovement. I do not argue that all
mood, drive, displacement, and vacuum acts - should be
(or most) of them lie within theoretical neuroethology proper,
resolvable as corollaries. So far, research on t h e neural
but only that they provide relevant concepts for the construction
underpinnings of FAPs has been regrettably very scarce,
ofa theory of neural mechanisms that addresses the integrating
probably because it takes a great deal of intensive reof action and perception in animal behavior. Hoyle says that
search before any single behavior can b e adequately
"laboratory neuroscientists should keep a close watch on
understood. But to progress, there is no alternative:
. . . theorists to make sure they keep to the facts and propose
valid experiments." I argue, however, that the brain theorist
Some choices should b e made now and backed with
has at least two roles: not only to construct tightly constrained
resolve. May granting agencies see t h e ultimate wisdom
models tied to quantitative experiments, but also to conduct
of supporting the endeavor.
gedanken experi~nentsto enrich our vocabulary for analyzing
animals in the laboratory and the field: What are the possible
mechanisms of depth perception? How might limb movements
bacontrolled? How can an animal learn from experience? The
latter models may be seen as exploring the "style" of the brain,
they are, I claim, as relevant to the understanding of the
Commentaries submitted by the qualified professional readershi will
be considered for publication in (1 later issue as Continuing Con~inen- human brain as is the study of invertebrates. Another dimension
tanj on this article. lntegratioe ouemiews ond syntheses are e.~pecially is what might he called "applied brain theory" - as brain
theorists collaborate with workers in robotics and artificial
intelligence to explore ways to make increasing use of parallelism in the next generation of cvmputer systems. My own
Neuroethology: A call for less exclusivity
overview of multilevel approaches to brain thcory is given in
and more theory
Arbib (1972; 1981); another argument for not restricting brain
theory to the consideration of detailed neural modeling only is
Michael A. Arbib
given by Marr and Poggio (1977).
Center for Systems Neuroscience, Department of Computer and
Szentagothai and Arbib (1975) provide both a fi~nctionaland a
Information Science, University of Massachusetts, Amherst, Mass. 01003
structural overview of the nervous system, then lay out expcriLessexclusivity. I share Hoyle's enthusiasm for neuroethology
mental and theoretical studies, presented at a Neurosciences
as a well-defined area of neuroscience that emphasizes animal
Research Program work session, on neural mechanisms for
Open Peer Commentary
C o m m e n t a n j l H o y l e : Neuroethology
stereopsis and on the role of thc cerebellum in the adjustment
and learning of motor patterns. The style of visual modeling
given there has been developed by Marr (1982) and his coworkers. Stent (1981) has lauded Marr's work as ifit were sui generis,
but it is, in fact, just one chapter in the dynamic field of
computer vision, which has seen much interaction among neuroscientists, phychophysicists, and computer scientists, and
which is ably summarized in the recent texts by Ballard and
Brown (1982) and Nevatia (1982). The proceedings edited by
Amari and Arbib (1982) contain Ito's report on current experimental support for aspects of the Marr-Albus model of learning
in the cerebellum; Amari's review of competitive and moperative aspects in the dynamics of neural excitation and selforganization; and the work by my colleagues and me on modeling neural mechanisms of visuomotor coordination in frog and
toad (see also Lara & Arbill 1983). Another important study of
visually gujded behavior is the work of Reichardt and Poggio
(1976) on visfial control of the behavior of the fly.
Hinton and Anderson (1981) offer a collection of papers on the
"connectionist" approach to both brain theory and artificial
intelligence, seeking to undcrstand how computations can be
executed quickly if they are distributed over a network of
parallel processors. Here the emphasis is on memory mechanisms, but subsequent work applies connectionism to problems
in vision and the control of movement.
As a body of work, these volumes chart the emergence of a
paradigm of "competition and cooperation in highly parallel
neural networks" that will greatly contribute to our growing
understanding of the neural mechanisms of animal behavior.
behavioral physiology. At t h e morncnt it is an opcn question
which of these two strategies is the more successful one.
Hence, one should not exclude one of them by definition.
3. Restriction to cellular events. Although I favor the singlecell approach in my own research, I am not sure that we will find
any generalizable statement at this Icvel. Perhaps such generalizations are only possible at the level of groups of neurons. As
an example, the walking movements of mammals and insects are
certainly not produced by the same kinds and numbers of
neurons, but perhaps by functionally similar groups of neurons.
As each science is only valr~ablewhen it produces statements of
some general applicability, oneshould not exclude by definition
a possible - eventually, the only possible - source of generalization.
Perhaps my view is wrong, and the elimination of these
aspects may not hinder future research. If the target article only
seeks to demarcate a certain kind of neuroethology from other
related disciplines, then investigators dealing with the aspects
mentioned above (as I do myself) would no longer be called
neuroethologists. This would be no disadvantage if it were only a
matter ofclassification, but I fear that such a line of demarcation
could also be used - in contrast to its original intention - to
establish new kinds of dogmatism and then to suppress new
ideas. In my opinion, therefore, it is too early to define acertain
segment of our discipline in such an absolute manner.
Flow diagrams and hydraulic models
Patrick Bateson
Neuroethology: An overnarrow definition can
become a source of dogmatism
Ulrich Bassler
Fachbereich Biologie der Universit6t Kaiserslautern, Federal Republic of
I like most sections of Hoyle's target article, especially the
historical parts (although the role of von Holst is not correctly
described), those dealing with the lack ofconcepts and theories,
and, of course, those favoring insects. I also agree that the
discipline that studies the neural basis of innate behavioral acts
should be defined and could be called "neuroethology." (In
Germany, the term Sensomotorik covers most of this field.) But
some aspects of the definition in the target article (sometimes
those only read between the lines) exclude topics of strategies
that could become relevant for this discipline in the future. Such
aspects are:
1. Exclusion of reflexology. Within the last 10 years a large
number of reflexes have been found in which direction or
intensity depends on the behavioral context (e.g., Bbsler 1983).
The more investigators have looked for such phenomena, the
more examples have been described. Perhaps the distinction
between reflexes and the release of FAPs will disappear in the
future, and reflexes can then be used as models for the release of
2. Exclusion of behavioral physiology (ethophyslology, Verhaltensphysiologie).The study of the neural basis of a particular
behavior can be started either from the higher level of complexity (behavior) or from the lower one (neurophysiology). The first
strategy can normally be divided into three stages: (a) quantitative description of the behavior (which can also be attributed
to ethology); (b) relating the behavior to the activity of one
system or a few unambiguously defined ones (in other words,
one tries to show that the behavior in question is a characteristic
ofa specified, but only functionally defined system); (c) elucidation of the neural basis of this system (for more details of this
strategy, see Bbsler, 1983). Stage (b) very often uses methods of
Sub-Department of Animal Behaviour, University of Cambridge, Madingley,
Cambridge CB3 BAA, England
~ o y l e ' approach
has something in common with the hydraulic
model he admires so much. It is provocative and amusing,
external considerations play no role in keeping it going, and, in
general, it is wrong. For all its defects, though, Lorenz's
hydraulic model hada numberofvirtues, as Hoyle rightly notes.
It was simple and vivid. It treated behavioural organisation as a
cohereyt system. Above all, it was a sofhvare account of how
behaviour might be controlled, not a proposal for what the
hardware might b e like. A flow diagram in more than one sense!
It would have been reasonable to expect that nobody would try
to relate the cistern's contents to some analogous fluid in the
central nervous system such as a neurotransmitter. No such
luck, since many people did.
Lorenz's model was unsatisfactory in dealing with feeding
behaviour for some of the reasons that Hoyle mentions, and it
was actively misleading in accounting for sexual and aggressive
behaviour (Hinde 1970). Hoyle hopes that he can deal with
these difficulties by incorporating some fancy-looking hardware
and some feedback circuits into the model. H e does not seem to
realise that he has lost the simplicity and vividness that made
Lorenz's model so attractive. Hoyle's updating is baroque,
unfalsifiable, and no better than numerous other models that
could be (and have been) devised. What is worse is that, like
others before him, he seems to be in serious danger ofbelieving
that the working parts of the model bear some straightforward
relationship to those bits of the nervous system that he seeks to
study as a neurophysiologist.
Although it is much less central to his interests, it is worth
noting that when Hoyle writes so glibly about innate behaviour,
he has wedded himself to yet another outmoded body of
thought. Even Lorenz (1965) abandoned the learning-instinct
dichotomy in the face of cogent criticism and drew a fresh
distinction between phylogenetically adapted and ontogenetically adapted behaviour. Behaviour adapted during the course
of evolution sometimes requires a learning process, such as
imprinting, during the development of a n individual. So
C o i n ~ w n t a r y l H o y l e Neuroethology
Lorenz's category of phylogenetically adapted bchaviour is not
the same as unlearned behavioiir. The notion of unlearned
behaviour is not implausible, providing one remembers that
"experience" in a general sense is inevitably involved as a
necessary condition in the expression of such behaviour. However, unlearned behaviour is not easily and unequivocally identified in practice, because to do so involves proving a negative.
Even if this difficulty is brushed aside, as it often is nowadays,
the belief that adult behaviour can invariably be dissected into
learned and unlearned components is certainly wrong (Bateson
1983). So is the conviction that behaviour is distributed bimodally into two clusters, one ofwhich is learned and the other
ofwhich is not. Hoyle's insects may not seem tolearn much, but
their capacity is easily underrated simply because nobody has
looked very hard for behavioural plasticity. When someone
does, the capacity for behavioural change may be greater than
naive preconceptions suggest.
Hoyle evidently looked at some modern textbooks on animal
behaviour and showed a draft of his article to practicing ethologists. Why did h e not heed their advice? I find it difficult to
believe that h e persisted in misrepresenting the modern state of
ethology through an obstinate sense of his own rectitude.
Perhaps the clue is to be found at the end of his article where he
refers to the support of granting agencies. Does h e knowingly
tell a misleading story in an attempt to corner meagre research
funds for his own brand of research? If so, he is wicked. But even
if that were the case, it would be difficult to be really cross with
him. Among physiologists, he is very unusual in wishing to link
his work with more complex levels of organisation rather than,
as he puts it, "leaning toward the principles of neurophysiology,
with its reductionism and intense concern for novel cellular
processes." I like that. Instead of biting the hand that is extended towards us, we ethologists should guide its owner to
problems that seem genuinely tractable to his neurophysiological skills. A question remains: Will h e let us?
Neuroethology: In defense of open range;
don't fence me in
Theodore H. Bullock
Neurobidogy Unit, Scripps Institution of Oceanography and Department of
Neurosciences, University of California, Sen Diego, La Jolla, Calif. 92093
Programmatic science is an old story. Before Hoyle, many
others with worthy goals have aimed at persuading, reasoning
with, luring and coercing scientists to choose their material and
their approaches toward a common problem. By and large, the
best science has been undirected and unfettered, whether by
choice of material o r approach or by someone's definition of the
preferred scope. I understand and emphathize with Hoyle's
goals. I sit at the same time in an oceanographic institution,
where some oceanographers would like everyone to work on the
oceans, and in a medical school, where some medics would like
more concentration on medical problems as they define them.
Fortunately for the standing of both, the prevailing policy is
broader, and the lesson of Julius Coinroe (1977) is accepted.
Comroe (see also Comroe & Dripps 1976) showed by historical
research that if you identify a series of advances in science,
chosen as the most important insights with respect to some
defined goal (medicine in his case; but we may substitute the
neural basis of species-characteristic behavior), the key research
that opened the way to those insights would, in a high percentage of cases, have been considered at the time so remote from
the area it eventually illuminated as to b e quite irrelevant.
This is my short-form comment on one of Hoyle's main points,
namely, that for key insights into the neural mechanisms of
locomotion we should work on locomotion, or at least animals
with legs! The whole history of biology is eloquent testimony
against such a restriction.
The other main point of the target article, namely, that
research should not be called neuroethology unless it is obviously centrally relevant, pales in cogency under this light.
What's in a name? Usage of the term "neuroethology" will vary,
in spite of Hoyle's considerable influence, just as perceptions of
its history and utility may differ (Bullock 1983). Sincc Hoyle is
aiming at neural mechanisms at the cellular and circuit levels,
the key insight might well come from spikeless neurons in crabs'
legs o r fish retinas, from plateau potentials or regenerative
repolarization in stomatogastric ganglia, o r from reciprocal synapses in rabbit olfactory bulbs. No one hoping for real understanding will be contcnt for long merely to search in a behaving
animal for the distribution of items on a list of known circuit
variables that has been frozen as of 1983 - given the spectacular
growth of that list over the years.
Like Hoyle, I find some approaches more exciting than
others; but unlike him, I hate toadmit it, and I try toovercoine it
- on.the sound old principle that you're down on what you're not
up on. Much of Hoyle's target article is a confession of preferences. In inany impassioned discussions the giveaway to the
presence of a question of taste, about which there is no disputing, is the phrase, "the question is . . ." - or the set of questions, o r the relevant approach.
But there is a position for which I have even less taste,
expressed as some form of, "Let us first understand this simpler
level and then investigate the more con~plex."I used to hear
that from biochemists and "general" physiologists who were
impatient over money spent on research of only special interest,
such as on flying in grasshoppers o r on the visual cortex - as
though the world would wait for them, and as though their
findings could simply b e scaled up to explain speech.
It is not simply tolerance of other people's approaches, levels,
and materials I am urging, but a genuine and humble appreciation of the absolute necessity, for the sake of t h e best science,
that the curiosity, ingenuity, rigorous thought, and creativity of
many scientists, with diverse talents and tastes, should be
encouraged to range freely! However, not to worry; even an
article in BBS won't stop them.
Difficulties and relevance of a
neuroethological approach to neurobiology
F. Clarac
Laboratoire de Neurobidogie Cornparbe, C. N.R.S.. Universitd de Bordeaux
1, 33120 Arcachon, France
Hoyle has always been a sort of barrister defendingand promoting behavior (1975; 1976; etc.). In this article he attempts to
make a synthesis of the ethological approach to animal activities,
particularly of invertebrates, with modern neurobiological studies. In a sentence, the paper states, it is time we knew what
neuronal systems are used for! This is true, and insufficiently
understood by neuroscientists, even by those whose speciality is
invertebrate studies. For most of them, invertebrate preparation is merely an isolated system useful as a membrane model or
for deciphering cellular mechanisms. A striking example of
such an attitude is presented by the studies on the swimmeret
beating in decapod Crustacea. Since the pioneering works of
Davis (1968), this preparation has been limited to a consideration of the connectivity of the different motoneurones, comparing the cellular membrane properties to analogous models. This
is, of course, useful, but it is curious that until now (Cattaert &
Clarac 1983), the relation of the beating and the behavioral
activity of the animal had never been studied. This is of particular interest if we remember that the swimmerets are a vestieial
locomotor system, which is no longer involved in displacement
(Bent & Chapple 1977). It was demonstrated that swimmeret
beating is linked to thoracic locomotion and, at the same time,
associated with very different behavioral situations. For each of
C o m m e n t u r y l H o y l e : Neuroethology
these, the number of muscles implicated, the frequency of the
rhythm, the amplitude of the movemcnts, and the forcc excrted
are different and characteristic of each situation. The role of this
heretofore ignored rhythm will soon be known. Several other
motor systems must be studied at this level of complexity in
order to make the association'betwcen a motor system and a
given behavior.
Since I fundamentally agree with the importance and the
scope of neuroethology as presented by Hoyle, my main comments will describe the difficulties encountered by such an
approach. When Hoyle edited a book entitled Irlentified Neurons and Behavior of Arthropods (1977) in honor of C. A. G.
Wiersma, the and was a very important detail. In the present
paper, the goal of the ner~roethologistseems to be to study the
neurons of behavior; this of course has to be done, hut several
dangers must be outlined.
By definition neuroethology is a "vertical" science, whose
main interest is to link the results obtained from many different
levels of complexity in the nervous system. We know that each
level has its own logicand its specific rule. When Hoyle presents
a general diagram of the jump (Figure 1) as a FAP, he does not
emphasize the behavioral laws regulating the motor processes.
A neuroethological diapam must incorporate adaptations to the
constraints of the environment. I disagree with the author's
contention that the circuitry of the jump has been worked out to
the exclusion of possible minor modifications. New neuronal
networks may yet b e found whose function is an expression of
We can reproach Hoyle for this aggressiveness in attacking
certain isolated neuronal preparations as being invalid material
for neuroethological studies while he himself proposes other
preparations that still have not reached the desirable level for a
neuroethological approach. When he later proposes that the
scientists working on mammals use slices, he becomes a reductionist (!), a criticism he must try to avoid.
Locomotion is involved in a behavior when we consider that
displacement is included in an oriented action, such as in
searching for a prey or a partner for mating. . . . In recent
reviews on this subject by Grillner (1'981)and Wetzel & Howell
(1981), the authors always took great care to distinguish the level
at which the results were obtained; an example in characterizing
this attitude is the success of the term "fictive locomotion," used
for the first time by Perret, Millanevoye, and Cabelguen (1972). In
itself, "fictive" does not have a very satisfactory meaning, but it
does permit one to consider all the work done on central pattern
generators and to propose a possible relation with the data
obtained from the intact animal. The question of the possibility
of making generalizations about data obtained at the cellular
level is enunciated by Sclvcrston in his BBS article, asking "Are
central pattern generators understandable?" (1980).
In order to link the different levels of neuronal complexity and
to give 11s a good idea of behavior we must: (1) have all the
parameters of behavior in our preparation, and not in the form of
a largely dissected and "pinned" preparation, just a poor imitation; and (2) work on the properties of the higher lcvel of
complexity that corresponds to the laws of behavior.
With that in mind, the explanation of some bchavioral laws
lies at the level of the individual cell, as dcmonstratcd by Hoyle
himself (1980); the tonically firing coxal adductor involved in the
leg-movement learning paradigm can be trained to fire at
different rates by operant conditioning controlled by a computer. In the same manner, when Kupferman, Cohen, Mandelbaum, Schonberg, Susswein, and Wciss (1979) defined the
metacerebral cell as an "arousal cell" controlling the feeding
behavior ofdplysin, they opened the large field of neuromodulation, which is particularly useful to a neuroethologist. [See also
Dismukes: "New Concepts of Molecular Communication
among Neurons" RBS 2(3)1979.]
The ensemble of neurobiology could be just an opposition of
several branches of science such as biophysics, biochemistry,
cell biology, pharmacology, physiology, or ethology, as a t the
annual meeting of the Socicty for Ner~roscicnce.If we refer to
the number of communications and posters under the heading
of neuroethology, we find that t h e neuroethologist is a rare
specimen! Because of the difficulty of the job, the neuroethologist must take the different parts ofthc nerlrobiological
puzzle and place them in their proper order, relating the lower
levels of organization to the more complex.
In order to obtain an adequate knowledge of neuroethology,
we need some conceptual approach that allows us to keep the
hierarchical complexity of neuronal organization. In considering
motor control, we have several models presented by "mammalian scientists," which are very instructive even for "invertebrate scientists," because their functional diagrams present the
order of complexity of neurobiology. MacKay (1980) and
Paillard (1960; 1983) offer some interesting approaches to the
organization of motor behavior. In his model, MacKay considers
motor behavior as a system of conditional loops with several
levels of instructions; the complexity of this hierarchical structure depends on its level of evolution. Then, even in the
simplest FAP, it is possible to consider a motor organization
sequence composed of the following elc~nents:selection of the
goal, selection of the muscles, timing the relation, force regulation; all these elements converge to permit a movement adapted
to the environment. This kind ofapproach preserves the behavioral level and leaves it in its proper place. This is the software of
a computer, whereas the majority of scientists only study the
There appears to exist among research scientists a kind of
gravitational force that compels them to explain their problems
in more and more detail. As their descriptions reach more and
more precise mechanisms, the behavioral aspect becomes less
and less evident. In opposition to these descending analyses, a
neuroethologist must have an ascending vision linking lowerlevel mechanisms with more integrated processes. Hoyle's
target article, then, is necessary, if it presupposes behavior as
the underlying basis of our work, but it misses the point, if it is
taken only as a justification of work done at the cellular level.
Neuroethology: Why put it in a straitjacket?
Jackson Davis
Fachbereich Biologic, Universitat Konslanz, 0-7750 Konslanz 7, Federal
Republic of Germany
As one of the earliest, most enduring, and least flappable
proponents of neuroethology, Hoyle deserves credit. His target
article serves the useful purposes of drawing attention to this
budding transdiscipline and outlining the views of one of its
most outspoken adherents. Especially laudable is Hoyle's call
for the de~elopmentof general principles of nerlroethoiogy (see
below). Beyond these broad generalizations, however, the present treatment is in major respects unsatisfying, leaving us with
many more questions than answers.
Perhaps the central unanswered question is why we should
attempt in the first place to define the scope of neuroethology.
Aside from creating arbitrary new labels and pigeonholes, it is
not clear what this exercise in intellectual territoriality accomplishes. Hoyle's purpose seems to b e to deny certain individuals
their righthl place in the Hallowed Halls of Neuroethology.
Hoyle thereb y reveals himselfas a scientificelitist. In contrast, I
am a populist. Let us open wide the Hallowed Halls to all who
would enter by defining neuroethology broadly and simply as
the study of the neural mechanisms of animal behavior. Much
needless time and argument can thereby be saved for more
substantive tasks, such as closing the present gulf between
biophysics and behavior. Any study that contributes to this end
is rightfully classified as neuroethology, including certainly the
elegant analyses of motor pattern generation by Selverston
ComtnentarylHoyle: Neuroethology
(1980) and colleagues (Selverston, Rnssell, Miller & King 1976),
and the classic studies on the neural and biophysical mechanisms of habituation and sensitization by Kandel and collaborators (Kandel 1976; 1979; Kandel & Schwartz 1982).
Perhaps the effort to build boundaries around neuroethology
could be justified under the banner of formulating broad new
goals and approaches to the topic. Hoyle's article contains much
that is broad, but little that is new. First, we are treated to a
highly personalized "history" of ethology, the purpose of which
is to provide a model for the development of neuroethology. The
history would flow differently from a different pen, but no
matter, for the parallels are not persuasive. Ethology developed
as a pioneering science, faced with a constant demand for
breaking new ground and establishing new principles in a
relative conceptual vacuum. The neurosciences followed a similar course, and are presently at a younger stage in their evolution. In contrast, neuroethology is a hybrid, the "progeny" of
' b o comparatively mature disciplines. The different etiology
renders a different developmental history inevitable; one cannot provide a model for the other.
When it comes to goals and approaches, one is left wondering
where Hoyle stands. From ethology h e draws the lesson that
success stems from focusing on "stereotyped, complex, nonlearned, innate behavioral acts," and he proposes that neuroethology d o the same. But in listing the goals of neuroethology, Hoyle identifies no fewer than 13 areas that deserve
attention:-beginning with neural circuitry, coursing through the
labyrinth of drive and motivation. and finally terminatine with
leaking and memory. I concur with the desGability of breadth,
but am perplexed by Hoyle's apparent inconsistency. Similarly,
his Abstract encourages the study of "diverse animals from
different phyla," but he suffers a later relapse into phylogenetic
chauvinism, with yet another plea for neuroethologists to focus
on Hoyle's choice of preparations, namely, "large insects" (read
"locusts"). The locust is without question a fine neuroethological preparation, but so are the sea slug, crayfish, lobster, praying
mantis, lamprey, the owl and the pussycat. Imagine the state of
neuroethology without the insights provided by studies on these
organisms! Diversity is prerequisite to evolution by natural
selection. Let us hope that diversity remains the basis of the
evolving science of neuroethology, diversity in technical and
conceptual approach, and diversity in the choice of experimental subjects. Long live hybrid vigor!
~oliticianshave develbped t h e strategy of making opposite
and contradictorv statements in order to avveal to the fullest
spectrum of opinion. In this sense, Hoyle's target article is a
success. There is something here for everyone, except perhaps
Aplydologists (take heart, Aplysia. Pleurobranchaea does not
even receive dishonorable mention). Hoyle's strongest suit is
his evident appreciation for general principles. The ability to
formulate unifying principles, that is, those that have application across many neurons, networks, and phyla, is one index of
the intellectual maturity of the discipline. Such principles furnish a conceptual framework for the design and conduct of
experiments, and they can represent the "larger questions"
Hoyle seeks for the "truly inquiring mind." As Hoyle recognizes, the field of neuroethology is ripe for such formulations.
We would do well to get on with the task, and to desist from
divisive and diversionary attempts to confine neuroethology to a
definitional straitjacket.
Can neuroethologists be led?
Fred Delcomyn
Department of Entomology and Program in Neural and Behavioral Biology,
Universify of Illinois, Urbana, 111. 61801
What we have here is a clarion call to arms in defense of the
emerging field of neuroethology. The question is, what is the
nature of the war?
On the one hand, if the target article is meant mainly to
establish a commonly accepted definition of an emerging field, I
think Hoyle is a general without an army. Fields are established
by bodies of workers who share common research goals and
methods. A developing field can be helped along by its workers
who help publicize its name and concepts, as Hoyle himself has
done in the titles of two reviews, "Cellular Mechanisms Underlying Behavior - Neuroethology" (1970) and "Identified Neurons and the Future of Neuroethology" (1975). Its content can
also be shaped by example, as Kenneth Roeder did before the
term even came into use (1963). But it cannot be directed along a
specific path merely by the opinions of a single individual.
Part of Hoyle's difficulty is that few others will share his
particular vision of the field. Hoyle seems to "know" what ought
to be part of neuroethology and twists and shapes his definition
until it fits his own mental image. Why else dismiss Ewert,'s fine
work ongrey-capture in toads as "comparative physiology," just
because analysis of the system has not yet reached t h e cellular
level? Why else include the simple movements that constitute
the jump of a locust while excluding the complex behavior
involved in kinesis? Is it just because w e have been able to
analyze jumping in terms of the activity of individual neurons,
while our understanding of kinesis has languished? I could give
other examples, but there is no sense in belaboring the point. In
the end, neuroethology will constitute the kind of work done by
investigators who call themselves neuroethologists, not just the
kind of work that a single individual believes should be
On the other hand, there are other factors that can shape a
field these days. If Hoyle's article is meant mainly as a device to
attract funding and recruits to the emerging field, then he may
indeed have a cause, but the campaign may be Like the Children's Crusade of medieval times. Hoyle's last sentence is, "May
granting agencies see the ultimate wisdom of supporting the
endeavor." But will they? And will researchers tackle the hard
problems Hoyle defines as the heart of t h e field? Jobs, grant
support, even peer recognition depend on a steady - some
might even say voluminous - output of research results. How
many researchers w e willing to invest 2 or 3 years in a difficult
project with the very real prospect of having little to show for
their efforts at the end? As long as all the stakes go to those who
can demonstrate rapid progress, Hoyle's attempt to lead his
colleagues into taking a longer view of their work seems to b e as
likely to succeed as were the youthful crusaders of so long ago.
One may applaud the effort, without much expectation of its
Disregarding vertebrates is neither useful
nor necessary
Gunter Ehret
Fakult&t fiir Biologie, UniversiMt Konstanz, 0-7750 Konstanz, Federal
Republic of Germany
If Hoyle's target article had closed with the paragraphs on
"Goals for neuroethologists," I am confident that it would be
widely accepted as presenting a consistcnt and sagacious review
of the foundations, limits. and aoals of neuroetholow. The
shortened article would not only have been in consonance with
Hoyle's own definition of neuroethology ("the study of neural
mechanisms underlying the behaviors that constitute the science of ethology," with ethology defined by Konrad Lorenz,
1981, p. 1, as "the comparative study of behavior, which applies
to the behavior ofanimals and humans") and with his illustrative
model of behavior generation (Figure 4), but also with recent
views of neuroethology summarized in Ewert, Capranica, and
Ingle (1983)and Huber and Markl (1983). For me, dissonance
within this article itself (see below) and with the opinions of
many other students in the field ofneuroethology (in the books
mentioned above) is introduced and provoked not so much by
C o m ~ n e n t u r ~ y l H o y l Neuroethology
locusts.The primary goal for neuroethologists, according to
stressing invertebrates, especially insects, as the first-choice
Hoyle, should be the "study of the cellular events underlying
animals to study within the rubric of neuroethology, but by (1)
fixed action patterns and related instinctive acts. " If one consults
concluding that neuroethological rescarch in vertebrates has
the ethological literature, one finds that neithcr locusts nor fixed
been irrelevant (or even nonexistent) so far, and (2) proceeding
action patterns (FAPs) are the main target of ethological reto set the rules by which behavior of vertebrates might fit (if at
search. In a recent textbook on the principles ofethology, even
all) into "true" neuroethological research.
Lorenz (1982) devotes more space to the modification of behavAnd all this because of seemingly necessary consequences
ior than to fixed action patterns. This apparent discrepancy
from the ethological side of ncuroethology! As little as the
probably has two causes: Hoyle's definitions are too narrow, and
science ofethology, as defined and discussed by Lorenz (1981),
the techniques of neuroethology restrict this discipline to a
is restricted to the observation and quantification of movement
small range of experimental animals and behaviors.
or fixed action patterns, the science of neuroethology has to b c
The model Hoyle proposes as a modern substitute for the old
restricted to the study of the neural circuits of such movement
Lorenz model [reproduced here as Figure 1 of Hoyle's accompatterns. There can be no doubt that ethological work encompanying Response, 9. u.] clearly states his primary interest in
passes the stimulus configuration for releasing certain semotor systems. His statement that an eminent ethologist does
quences ofmovement (sign or key stimu1i)as well as internal and
not take the old Lorenz model too seriously any more could refer
external modulatory influences on and learning and memory in
to Lorenz himself, who has published a modified version of his
the execution of, for example, prey-catching, courtship behavmodel that differs markedly from the old one (Lorenz 1982).
ior, mating, and brood care. The neural bases of all such
This new model assumes that t h e releaser docs not act by
complex, goal-related, naturally occilrring behaviors, which can
opening the spring directly, but that it fills the reservoir tobe described by Hoyle's model (Figure 4) and which arc in
consonance with his "Coals for ncuroethologists," have I ~ e c n gether with a number of "charging" and endogenous stimuli.
Hoyle's model, in my view, is a detailed description of the water
pursued in vertebrate research, which, consequently, has to b e
trough of the Lorenz model. It is rcmarkably vague about the
called neuroethological work. Studies on bats, electric fish, and
function of the comparator and computer. As the software of the
barn owls, especially, which are disregarded in Hoyle's article
computer is not described, I cannot see how this model could be
for being too specialized, have highlighted principles of neural
tested experimentally.
representation of stirnrilus parameters and feature extraction in
The central problem of neuroethology is whether an analysis
the brain, which are necessary prerequisites for initiating and
of the neural mechanisms controlling natural behavior is possiguiding a behavioral sequence toward its goal (e.g., catching
ble at all. The li~nitingfactoris not whether an animal has legs or
prey). Although we have to admit that, as Scheich (1983, p. 8)
whether it is a "glob of squishy protoplasm," but whether it
says, "the art of neuroethology of vertebrates is hardly beyond
performs the behavior under the restricted experimental condithe stage of a comparative neurology of sensory systems," these
tions of a neurophysiological experiment. T h e logical starting
sensory systems are (1)equally part of Lorenz's hydraulic model
point ofa neuroethological analysis has to be a careful observaofbehavior generation and, as I understand it, are (2) investigattion of the behavior under natural conditions. The next necesed with the ultimate goal ofgetting insight into the generation of
sary step is a behavioral analysis under laboratoty conditions.
a certain behavioral sequence that often is, in fact, a fixed action
And this is when the problems begin. In most cases, laboratory
pattern, and (3) lead, on a comparative basis, to well-coordibehavior differs significantly from free, undisturbed behavior
nated approaches of sensory-motor interfacing in vertebrates.
It is therefore clearly inconsistent (and herein lies the inunder natural conditions. If the experimenters proceed at this
point with the analysis, they have to be aware that the neural
coherence of the article) that, on the one hand, neuroethology
and its goals are discussed in a comprehensive way, and, on the
mechanisms they are going to study apply to behaviors that are
only loosely correlated with the original natural behavior. Neuother, the scope of ncuroethology is restricted mainly to insect
roethology, in my view, presently analyzes in a first crude
It may be easier for neuroethologists involved in invertebrate
approximation the real neural events that control natural behavior. For many behaviors, it will b e i~npossibleto perform a
work to wear all the hats of physiology, biophysics, and bioneuroethological analysis. O n e example is the waggle dance of
chemistry at the same time, because they are dealing with
systems with only a relatively s~nallnumber ofclemcnts. Possithe bee. Unlike Hoyle, I do not see a possibility ofstudying this
form of communication with neurophysiological techniques,
bly, progress can be made faster and thus the goal (of undersimply because a bee does not exhibit it under laboratory
standing a certain behavior) can be more obviously linked to
every publication of results. The investigator of complex verteconditions.
Another point where I disagree with Hoyle is in the emphasis
brate behavioral sequences is more likely to be forced to wear
the hats one after the other and to work for subgoals that,
he puts on the analysis of the motor system and the secondary
together with work in other laboratories, can add up to major
role h e assigns to the analysis ofscnsory information processing.
progress in understanding animal behavior. But insofar as the
The functional role of a releaser and the mechanisms of eliciting
a specific behavior with specific stimuli can only be understood
biology of behavior is the principle that guides the research
after performing a careful analysis of the processing of sensory
through the labyrinth of the different methodological apinformation at the level of the receptors and higher-order
proaches and subgoals, there is no obvious reason the research
interneurons (Boeckh & Ernst 1983; Huber 1983). Exclusion of
should not b e termed neuroethological. A flourishing and widesensory physiology at the different neuronal levels is such an
ly recognized neuroethology cannot be restricted to invertebrates or to the study only of motor coordination. The major goal
extensive restriction that w e ought to rename this discipline
"motorethology. "
of neuroethology is, as Huber (1983, p. 91) says, "to provide an
understanding of behavioral strategies of animal spccies in
terms of operations of their nervous systems at all levels."
Neuroethology or motorethology?
Joachim Erber
hstitute of Biology, Technical University of Berlin 1000 Berlin 10, West
After reading Hoyle's article, I had the impression that "real"
neuroethology deals with the study of motor systems in
Hoyle's new view of neuroethology: Limited
and restrictive
J.-P. Ewert
Neuroethological and Biocybernetics Laboratories, University of Kassel,
0-3500Kassel, Federal Republic of Germany
Hoyle points out that neuroethology could not have been
developed before ethology was established and ethological concepts had bcen worked out. This argument is reasonable in one
CommentarylHoyle: Neuroethology
respect (Ewcrt 1984), although I would agree with the broader
view put forward by Bullock (1983), namely, that neuroethology
did emerge from an eclectic confluence of many streams originating from a wide assortment of traditions of ethology, comparative physiology, comparative neuroanatomy, ant1 clinical
neurology. In this context, I am greatly surprised that Hoyle
devotes more than 10% of his target article to the description
and discussion of Lorenz's hydraulic model, even saying, "The
toilet model has come to symbolize neuroethology. In no place
does he mention the pioneering work by C. A. G. Wiersma
(1974), who has shown us how to discover individual, rccognizable, and behaviorally meaningful nerve cells, thus laying the
foundations for neuroethology.
Hoyle, calling himself "a dyed-in-the-wool champion of first
finding out how invertebrate nervous systems work," strictly
distinguishes among neuroethology, ethophysiology, and Verhaltensphysiologie, but unfortunately gives no definition for the
latter two disciplines. A main point in Hoyle's definition of
neuroethology seems to be the type ofbehavior under investigation; that is, neuroethology should not he concerned only with
"the neurophysiological fundamentals of behavior" and also no
longer with "the cellular mechanisms underlying behavior (cf.
Hoyle 1970)," but now with "the study of the cellular events
underlying fixed action patterns."Again, I think that this view is
too narrow and much too dependent on the definition of FAP,
which is itself disputed. Hoyle himself seems to invalidate his
concept by pointing out that FAP sequences may incorporate
reflex sequences; and then we are in trouble because he suggests excluding reflexes from neuroethological investigation.
But how can one know whether a behavior is a FAP or a reflex
without analyzing the neuronal circuitry?
Regarding the working program, Hoyle points out that neuroethologists will encounter novel as well as traditional membrane processes down to the level of ion channels. Some paragraphs later in this target article h e denies the value of related
data for ncurocthology, if they have been obtained in Aplysin since the investigated behavior docs not - according to Hoyle represent the kind of behavior that constitutes the science of
ethology. Is it because these animals "lack limbs"? Hoyle
himself began to think of the possibility of a science of neuroethology when he found that the leg neuromuscular junctions
responsible for marching behavior in grasshoppers were affected by the ionic composition of the blood. The realization that
the neural output was recordable and quantifiable was for him
approach (although
already the beginning of a neuroetho~o~ical
he was aware at that time that the behavior he was invcstieatine
had only some aspects of a FAP). Thus, h e emphasizes the
recordings of rnyograms and muscle potentials from the legs of
freely moving grasshoppers, pointing out, "This line ofwork has
since been developed by many investigators to the state ofa fine
art." The jamming avoidance response ofweakly electric fish, on
the other hand, does not appear to b e adequate for neuroethological research in Hoyle's view, since, as he says, "as
'behavior' [it] is highly specialized" and "does not involve limbs,"
albeit he realizes that "the motor aspect - generation of the
discharge - is quantifiable, and the sensory return is addressable all the way into the brain."The possibility that, for example,
our knowledge of behavior-related neural principles obtained in
electrosensory systems of these specialists (e.g., time domain
analysis of frequency-related inforlnation by coincidence circuits) might contribute to the understanding of gencral rules
(e.g., in auditory systems) is not considered by Hoyle.
The main goals of neuroethology listed by Hoyle are not much
different from the ones described elsewhere in the literature of
vertebrate neuroethology, except that he has partly reversed
the sequence (priority?) of the topics. Indeed, invertebrate
neuroethology and vcrtebrate neuroethology tend to use diffcrent research strategies. Whereas the first often approaches the
functional properties of neuronal networks controlling behavior
from the motor side, the latter has first focused its interest on
sensory and motivational aspects. Of course, therc is no right
place to begin, since all are parts of an integrated whole (cf
Hoyle 1977). In this context, I think, the analysis of the sensory
and motor aspects of releasing mechanis~ns- innate, modified
innate, or acquired - is an important task of neuroethology,
since it involves studics on the neuronal basis of (1) stimulus
feature extraction, (2) stimulus localization, (3) sensorimotor
interfacing and feedback interaction, (4) modulatory functions
and storage processes, and (5) motor pattern generation. Hoyle
avoids the term releasing mechanism, although it is linked with
an important concept of ethology (Schleidt 1962). He even
suggests excluding sensory physiological research from neuroethology, but at the same time he correctly realizes that "the
triggering of many FAPs depends upon feature extraction, so
releasing cannot b e fully understood without knowing the details of this subsidiary action," and some pages later he even
emphasizes that it is "only the extracted key features that
seriously concern behavior."
Regarding the question of how the central nervous system
works, Hoyle considers some basic ideas of the "command
system concept" introduced by Kupfermann and Weiss (1978)
under his new labels "keyboard" or "orchestration/modnlator"
action; we had applied these to the prey-catching sequence
(multiple-action system) of the toad: "Operation of each command system requires simultaneous activation of all of its command elements" (i.e., tectal output neurons with recognition
properties like class T5-2, neurons with localization properties
like classes T1 and T3, and neurons with arousal properties like
class T4).
Command systems differ from each other by a distinct combination of
command elements ()which can be shared by thedifferent command
systems [ I , forexample [(T4)(T5-2))- ORIENT, or[(T5-2)(T1-3)
(T3)]+ SNAP. . . . An AND-condition between two command
elements subserving similar functions might be altered to an ORcondition based on learning or due to the influence of other modttlatory elements. (Ewert 1980, pp. 125, 299-300)
Evidence that the'classes of tectal neurons mentioned above
project down to the motor systems (putative motor pattern
generators) has been provided recently by antidromic activation
of these cells in response to electric stimulation applied to the
tectobulbar/spinal pathways at the level of the caudal medulla
oblongata (Satou & Ewert 1984).
I think that Hoyle misses or misinterprets an important aim of
neuroethology, that is, the exploration of neural principles in
animals of different ecological and behavioral adaptations. The
comparative neuroethological approach - in particular, including those animals that are adapted to extreme environmental
conditions and have developed special strategies - may contribute to the understanding of general rules and concepts. As
predicted by Bullock (1983), we are going to realize that investigating interspecies differences in terms of neuroanatomy, neurophysiology, and ethology - including their ontogenetic developments - will provide important insight into general neurophysiological principles underlying behavior.
Neuroethology according to Hoyle
Russell D. Fernald
Medical Research Council, London WC2B 5RL, England; on leave lrom
institute of Neuroscience, University of Oregon. Eugene Oreg. 97403
Neuroethology is an emergent discipline in which the rich
collection of methodologies from the study of the nervous
system and the brain are applied to scientific questions derived
from careful behavioral observations of animals in their natural
habitats (Fernald 1984). Most scientists are engaged in neuroethological research as a result of pursuing interesting scientific questions beyond the narrow boundaries ofconventionally
defined disciplines, which are often characterized only by a
collection of related techniques (e.g., neuroanatomy, neurophysiology, etc.). Hoyle, with characteristic evangelistic zeal,
C o m m e n t a r y l H o y l e : Neuroethology
argues that certain neuroethological research directions, when
carried out on his favorite organisms, large insects, are intrinsically more worthwhile than others. H e offers, in support of this
idea, a highly selective "history" of the development of ethological ideas, spiced with self-congratulatory reminiscences.
Although Hoyle personally has played an important role in the
field of neuroscience through the analysis of neural circuitry of
identified neurons in insects, as well as by training several
students who are now productive neuroscientists, this discussion of neuroethology is seriously wrong in several regards.
First, Hoyle's summary of the history of ethology excludes
many significant contributions and exaggerates others, resulting
in a very distorted perspective on current ethological thinking.
For example, Lorenz's hydraulic model was a conceptual construct summarizing Lorenz's views about the organization of
endogenously generated behavior, and was intended to motivate other scientists to begin thinking about the immediate
causation of such behavior. It was not a model covering the
"generation of instinctive behavior" in its entirety, but an
attempt to schematize the motivational forces postulated to
underlie certain behavioral acts. Discussions of the applicability
and generality of this model certainly stimulated ethological
thinking by providinga focus for observational and experimental
analysis. The model has been supplanted in time by more
intricate representations based on more data about the many
influences on the behavior of specific animals (e.g., BaCrends
- -,
In urging neuroethologists to elucidate the neural equivalent
of an updated hydraulic model, Hoyle misses one of the important lessons to be learned from discussions about the Lorenz
model: There is no generally applicable description of the forces
underlying "animal behavior." Rather, the enormous complexity and diversity of the behavior of animals requires specific
models for analysis of specific issues. For interested readers,
Hinde (1982) offers an insightful, balanced analysis of the relationship between ethology and other scientific disciplines, identifying the complementarity and convergence of ideas from
different disciplines.
Second, Hoyle offers six terms as the key concepts of ethology, when in fact these terms are neither of acomparable level
for discussion among themselves nor do they represent the
"core of strictly ethological knowledge" as claimed. The undisputed contribution of the ethological pioneers, most notably,
Lorenz, Tinbergen, and von Frisch, was to recognize important
central principles in the otherwise bewildering complexity and
diversity of animal behavior. The first was that there is selective
responsiveness to particular stimulus characteristics known as
sign stimuli. Sign stimuli may be called releasers if upon seeing
them the animal consistently performs particular behavioral
acts. The second was the discovery that each species has stereotypical movements, termed fixed action patterns, which are
as characteristic of the species as are morphological features.
These correspond to Hoyle's numbers 3 and 1. The remainder of
the terms listed by Hoyle are of quite a different nature.
Displacement activities (2) are behavioral patterns that appear inappropriate or irrelevant for a given situation. Displacement activities need not be fixed action patterns, as Hoyle
claims, and are interesting primarily as a window into the
motivational state of an animal in a conflict situation. It is not a
central concept of modern ethology, but a descriptive term
primarily of interest to ethologists studying the immediate
causes of apparently irrelevant behavior.
Vacuum activity (4) and consummatory acts (5)are also terms
of limited use and usefulness, each describing categories of
events, not central principles of modem ethology. Finally, the
terms "drive" and "mood" (6) are qualitative descriptors of the
inferred state of an animal. While early investigators emphasized the importance of the internal state in understanding what
animals do, definitions of drive and mood are certainly not at the
core of ethological knowledge.
Finally, I strongly ohject to the suggestion that ncuroethologists should follow the goal.: laid out by Hoyle and by
implication adopt his unjustified prejudices against certain research directions. Whereas goal-directed scientific research
may be the modus operandi for attacking major commonly
agreed upon medical problems, basic research in general and
neuroethological studies in particular d o not fall into a similar
category. The major task of scientists is not to find the solution to
questions adopted from a list of chosen goals, but to select only
the most important questions to pursue from t h e many that one
confronts in scientific work. In this context, I am particularly
concerned by Hoyle's loudly proclaimed bias against research
on Aplysia. Pace Hoyle, detailed studies on various aspects of
Aplysia have led to important discoveries that are highly relevant to neuroethological inquiry, including studies of the neural
basis of learning (Carew, Abrams, Hawkins & Kandel 1983).
More recently, control of an important "real" behavior in
Aplysia, namely egg laying, has been traced to the genome
(Scheller, Rothman & Mayeri 1983).
Arguing from this same narrow perspective, Hoyle claims
that studies on vertebrates have provided little ofuse in the past
and promise little in the future for neuroethology. That this is
patently wrong should b e evident from t h e literature, but let me
offer one example. Hoyle argues that one goal of neuroethology
should be the elucidation of the efference copy. A neural
representation of efference copy has in fact been found in
vertebrates - fish (Bell 1981). Moreover, evidence for efference
copies is amply available in other species as well (Angel 1976;
McClosky, Colebatch, Potter & Burke 1983; Zaretsky 1982).
In conclusion, Hoyle's myopic view of neuroethology offers
little useful information or guidance for scientists interested in
understanding the machinery of the nervous system responsible
for initiating or modulating behavioral acts important for survival of the animal.
Neuroethology and theoretical neurobiology
Stephen Grossberg
Center for Adaptive Systems, M~thematicsDepadment, Boston University,
Boston. Mass. 02215
Hoyle's leadership role in neuroethology is well represented by
his list of 13 sensible and important goals that h e has targeted for
neuroethologists in the years ahead. This list reflects his clear
appreciation of the fact that "what is needed is focus on both
behavioral and neural circuit functioning."
This enlightened atmosphere is darkened by the remarks that
Hoyle directs against all vertebrate experimentalists. After
noting Ewert's definition of behavior (1980) as "spatially and
temporally coordinated patterns of movement," Hoyle blasts
the entire vertebrate field with the statement that "this may be
the best that can b e hoped for from studies on vertebrates." This
remark reflects a serious breakdown ofscientific communication
between behavioral and neural experimentalists who stud y
differeni organisms, or even different systems within the same
organism. This type of breakdown is inevitable when an experimental science does not have at its disposal theories powerful
enough to bridge the gap between its distinct experimental
paradigms. Hoyle clearly realizes this through his use of quotations such as "Experimentation in this area cannot proceed
without theories.
Hoyle goes on, however, to make the inaccurate claim that
"in the 34 years since t h e Cambridge meeting, there has been
little advance in its [neuroscience's] conceptual underpinnings.
The single general framework that has ever existed [was] the
McCnlloch-Pitts (1943) . . . model: . . . But the vacuum left
behind has yet to be filled with even a tentative new model."
Coming from an experimentalist of such distinction, an attack on
C o ~ n ~ n e n t a r y l H o ~Neuroethology
the huge field of vertebrate experimental studies and a total
ignorance of recent theoretical progress may b e viewed as
serious problems for the field as a whole. I believe that they
reflect the same problem.
Due to the complexities of behavioral and brain data, most
experimentalists have retreated into experimental paradigms
that are sufficiently narrow to support a "personal replication"
criterion of truth: If you don't believe or understand a piece of
data, you can then at least do the experiment over for yourself.
O r you may trust the results of a small group of colleagues who
studied with the same respected teacher, worked at some time
in the same lab, and so on. Given a personal-replication criterion of truth, data from other paradigms tend to b e ignored as
irrelevant, and an appreciation of theories capable of unifying
several paradigms becomes inconceivable.
To illustrate how different the data and theoretical landscape
look to me, I will briefly comment on some theoretical results
that are relevant to both invertebrate and vertebrate studies.
One sweeping claim deserves another. Significant theoretical
progress has already been made on all of the 13 topics that Hoyle
targets for neuroethology. Moreover, the theoretical principles
that support this progress enable specialized circuits to be
derived and used to analyze both vertebrate and invertebrate
data. A few recent examples and two older examples of this
theoretical progress will illustrate my claim.
Theoretical work on the neural mechanisms underlying reinforcement, drive, and incentive motivation led to a theory of
opponent processes, called gated dipole theory, in which slow
chemical gating reactions (e.g., involving norepinephrine) modulate cellular reactions to rapidly varying phasic cues and tonic
arousal shifts (Grossberg 1972; 1975; 1982b; 1 9 8 2 ~1983).
opponent processes were interpreted as simple models of hypothalamic circuits. Contrary to Hoyle's claim that "water . . .
represents basic but still unknown neurophysiology," these
circuits are part of a larger brain-behavior theory that addresses
all of the issues raised by the water models in his Figures 3 and 4
(Grossberg 1982a). My theory does not merely mimic a water
analog. For example, it disagrees with such claims as, "Drive is
the probability of occurrence of an appetitive FAP." This statement implies that a hungry animal will attempt to eat with equal
probability in the presence or absence of food. In my theory,
incentive motivation is closer to the concept that Hoyle seems to
intend: It is sensitive to a number of factors other than drive,
notably, the reinforcing properties of sensory cues, and the
competitive balance that exists among all external cues and
internal drives at any time.
With the appetitive hypothalamically interpreted circuits of
gated dipole theory as a starting point, G. A. Carpenter and I
realized that a specialized gated dipole circuit has circadian
clocklike properties. We have now quantitatively simulated
many of the important data that are ascribed to the circadian
pacemaker in the suprachiasmatic nuclei of the mammalian
hypothalamus (Carpenter & Grossberg 1983a; 1983b; 1984a;
1984b). Carpenter and I also realized (Carpenter & Grossberg
1981; 1983a) that an intracellular gated dipole process, in which
the gating chemical models an intracellular C a + + process, can
quantitatively fit parametric intracellular data that were collected from turtle cones (Baylor & Hodgkin 1973; 1974; Baylor,
Hodgkin & Lamb 1974a; 1974b). Putting together findings on
photoreceptors and circadian rhythms, it is now clear, at least
formally, how an intracellular gated dipole circuit of the photoreceptor type can b e modified to create a circadian pacemaker
circuit. A circadian pacemaker has, for example, been reported
in the eye ofAplysia (Jacklett 1969). Thus, a theory now exists in
which a general design principle and sharply articulated circuit
instantiations of this principle have contributed to the explanation of complex data about photoreceptor transduction, circadian rhythms, and motivated hehavior across several species. Of
particular interest to neuroethologists is the fact that these
results derive from an analysis of how the behavior of individual
organisms adapts to environmental contingencies on a momentby-moment basis.
Another recent theoretical contribution of this type was made
with my colleague Kuperstein (Grossberg & Kuperstein 1984), a
contribution to motor control whose significance again cuts
across neural systems and species. The behaviors in question are
saccadic eye movem nts. In consitlering these movements, we
had to derive explicit circuits for the computation of efference
copy, as well as many other processes that are of general
importance in motor control. This work illustrates one reason I
disagree with Hoyle concerning the claim that invertebrates are
always simpler to understand than vertebrates. Neuroethology
teaches us that neural circuits are organized to generate adaptive goal-oriented behaviors. Without a behavioral linkage, no
amount of superb neurophysiological experimentation can lead
to an understanding of brain design, becar~sethis type ofwork,
in isolation, does not
e probe the functional level on which an
organism's behavioral success is defined. Vertebrate behavioral
experiments are much more plentiful than invertebrate experiments - there are thousands of them on every conceivable topic
- and vertebrate behaviors are often highly strr~cturedand
paradoxical. These data provide just the type of structure and
paradox that force theoretical conclusions when they are confronted by a prepared theoretical mind.
As an active theorist myself for 25 years, I am eager to study
good data from all paradigms. As a matter of historical fact,
however, most of the anatomical and physiological results that I
have read in the invertebrate literature were already familiar to
me from theorizing about vertebrate data. Nevertheless, the
elegance and clarity of a completely worked out invertebrate
circuit is a thing of beauty and a joy forever. I still believe,
however, that the greatest benefits from invertebrates will
derive from their suitability for a biochemical analysis of learning and memory on the intracellular level. Working out acircuit
is just a preparatory step, albeit one that requires great imagination and virtuosity, for identifying the cells on which a biochemical analysis should be carried out.
To illustrate my claims about prior familiarity with invertebrate results and, more generally, that theoretical life has gone
on for some time since McCulloch and Pitts (as also is indicated
by several thousand pages in print), note how theory bears upon
some important recent experiments about Aplysia.
A major issue in psychology and neuroscience concerns the
relevance of invertebrate learning studies to the understanding
of vertebrate learning, notably human learning. The important
invertebrate studies of Carew, Hawkins, and Kandel (1983),
Hawkins, Abrams, Carew, and Kande1(1983), and Walters and
Byrne (1983) have bridged the gap between experimental facts
and theoretical models concerning the ncural substrates of
associative learning. The theoretical models suggest that the
cellular mechanisms of learning disclosed by these experiments
may be universal, but the anatomies in which these mechanisms
are expressed in invertebrates and vertebrates may differ in
important ways. One illustrative difference is indicated below in
the context of a general associative prediction.
On the mechanism side, the experiments support a 1968
theorctical prediction (Grossberg 1968; 1969a) that the action of
an unconditioned stilnulus (US) on prcsynapticconditioningofa
pathway activated by a conditioned stimulr~s(CS) is mediated by
a C a + + current. On the anatomical side, Hawkins et al. (1983)
suggest that a US activates a facilitator neuron that presynaptically modulates each CS-activated synaptic knob. In neural
systems wherein secondary conditioningcan occur, aconditioning experiment enables a CS to act like a US in later conditioning
experiments (Wike 1966). If the anatomical substrate of conditioning were universal, then every such C S could activate a
facilitator neuron that could modulate all the CSs with which it
could he conditioned. The wiring diagram of Walters and Byrne
(1983) accomplished part of this requirement by letting the US
activate a single facilitator neuron that nonspecifically moduTHE BEHAVIORAL A N D BRAIN SCIENCES (1984) 7:3
CommenturylHoyle: Neuroethology
lates the excitability of all CS-activated synaptic knobs. Their
network confirms a 1969 theoretical prediction (Crossberg
1969b; 1971; 1975; 198%).
A secondary conditioning capability also requires an anatomical feature that is not reported in the invertebrate experiments.
In order to acquire US properties, a C S must send a conditionable pathway to its facilitator neuron. The CS must b e able to
effectively activate this pathway after learning occurs but not
before learningoccurs. Hawkins et al. (1983 p. 403) report that a
C S cannot activate a facilitator neuron because "paired presentatioh of the C S and the US produced no more total firing of the
facilitators than did unpaired presentation. " Their observation
is compatible with a general prediction that is of independent
interest and whose verification would imply that the anatomical
substrate of conditioning reported in the invertebrate studies is
not universal: Either a neural system is incapable of secondary
conditioning, or a CS will cause increased total firing of its
facilitator neuron as CS-US pairing continues.
Thus, two of the most important recent experimental findings
aboutAplysia were theoretically anticipated 15 yearsago. Many
more theoretical predictions have recently received experimental support. One can only speculate how different the mind and
brain sciences would be today if the available means of theoretical communication, unification, and prediction were already assimilated by the experimental community.
Preparation of this article was supported in part by the Ofice of Naval
Research (ONR-N00014-83-K03.37).
Can the aims of neuroethology be selective,
while avoiding exclusivity?
D. M. Guthrie
Depamnent of Zoology, University of Manchester, Manchester M13 9PL.
Hoyle's intention in trying to place well-defined targets before
neuroethologists is a timely one. Unfortunately, his enthusiasm
leads him to propose such a wide variety ofgoals that the result is
inevitably rather confusing. His 13 goals seem to cover most
aspects of behavior, including s o far totally intractable ones, like
His remarks on vertebrate neuroethology are especially baffling, as despite a number of successful single-neurone studies
on vertebrate brains, some of them i n animals with a degree of
movement (Evarts 1976; Markowitsch & Pritzel 1978), Hoyle
persists in seeing the only hope for further advance in brain
slices. Indeed, one begins to suspect that it is the success of
vertebrate neuroethology as evidenced by recent publications
like Advances in Vertebrate Neuroethology (Ewert, Capranica
& Ingle 1983) that has led him to conduct a rearguard justification of invertebrate (that is to say, insect) studies. The hard fact
is that ethology has been largely founded on the study of
vertebrates,-whose well-ordered and easily observed behavioral
sequences have offered hope of analysis, in the first instance, by
behavioural methods. Most of the animals referred to by Tinbergen (1951) and Manning (1972) and cited in Table 1 are
vertebrates - 70% and 76% of t h e samples respectively - and it
is easy to see why this is so. Paradoxically, Hoyle's strongest
condemnation is reserved for the humble sea hare Aplysia "this behaviorally boring glob of squishy protoplasm." An internationally known pharmacologist who works mainly with mammals remarked, after hearing Kandel talk recently at Cambridge, that this was in his opinion a uniquely valuable system.
Like many of us he was mainly impressed by the positive aspects
of Aplysia research.
Over the question ofcell size and its effect on t h e accessibility
of neuroncs to electrophysiological techniques, it is worth noting that most nervous systems, including that ofAplysia, contain
some relatively small cells (say, less than 20 p,). As Hoyle
suggests, it would be interesting to know what goes on in the
insect brain, but one is put off by the d~ficultyofstudying the 25p, globuli cells that compose many significant structures like
the corpora pedunculata. In the fish I currently study, neurones
~ 3 0 ~to) the 4-5p
range in size from the Mauthner cell ( 4 0 0 by
cells of the optic tectum. At present, there is unavoidable
variation in the degree ofdetail we can resolve at different points
in such systems.
If neuroethology is to make progress, a pragmatic approach
must be fostered, that is, one aimed towards practical outcomes.
Systems that mediate limited and well-defined behaviours and
that offer rea~onablehope of detailed analysis at the neurone
level should be a prime object of study in whatever organism
they appear. I believe Hoyle is right when he says, "The time
required to describe a nervous system adequately is something
new to science," and I would agree that the FAP occupies a
central position in neuroethological thinking. I t is nevertheless
possible that the FAP will prove something of a millstone when
the freer, more exploratory types of behaviour come within the
scope of neurophysiological analysis.
The suggestion that systems engineers, robotics designers,
and artificial intelligence (AI) technologists, together with the
odd Nohel prizewinner in physics, might be useful in giving
some theoretical backbone to neuroethology is an attractive
one. Hoyle rightly stresses the information-processing side of
neuroethoiogical problems. In my (limited) experience, information technologists exhibit rather varied reactions to the idea
of collaboration with biologists. Some A1 researchers find such
contacts interesting and potentially valuable, like those working
on the OMS vision system (Brown, Boveri CSr Cie 1982-83);
others design information-processing stages that turn out to be
very similar to those proposed for biological systems. The
parallelism between the Ohta image analysis system (Ohta 1982)
and the processing steps suggested by Marr (1982) for human
vision may b e taken as an example of the latter; a t the same time,
the Alvey report, signalling a new initiative in information
technology in the United Kingdom, specifically excludes collaboration of this kind.
The value of the recent initiative that has occurred under the
label of neuroethology is that it has concentrated the minds of
those whose main aim is to elucidate the neuronal substrates of
behaviour, towards the idea of working on particular welldefined examples of behaviour. It has also had the effect of
making them pay some attention to the methods and goals of
ethologists, with ethology's inevitable bias towards the study of
Generalized model systems, like that of Lorenz and the
updated version put forward by Hoyle here, are often useful
mainly in providing material for review articles. They are
usually insufficiently specific to have very much predictive
force. For example, the quantified ideas concerning feedback
and feedforward seem to have come from servosystem engineers and applied mathematicians (Black 1934; Nyquist 1932;
West 1953) originally, and were then imported into physiology
(Bayliss 1960; Merton 1953) after further development through
automatic gunnery control systems (1939-1945). In this example, the electrical and mechanical ideas were disseminated in
engineering circles at first, and had little effect in telling biologists what to look for; but once the analogy had been grasped,
the ideas proved seminal for the interpretation,of the corpus of
knowledge concerning spinal reflexes that had accumulated by
Hoyle's orchestration/neuromodulator hypothesis underlines our present interest in neuromodulating substances, but it
is not clear from the model whether each substance corresponds
precisely to a major section of taped programme, or whether it is
simply producing what used to be called "set," predisposing the
CommentarylHoyle: Neuroethology
animal to a certain type of behaviour in a persistent way. The
octopamine example would indicate the former. 1 would agree,
though, that the opening up of research in the field of neuropeptides and similar substances offers an especially exciting prospect for neuroethology.
Ethology has progressed
Robert A. Hinde
Medical Research Council Unit on the Development and Integration of
Behaviour, Madingley, Cambridge CB3 BAA, England
In attempting to understand the diverse phenomena of the
living world, scientists must elasslfy them into manageable
groups, and they may use explanatory concepts whose utility
subsequentl y turns out to b e limited to a small range of phenomena o r to a particular level of analysis. The progress of
scientific understanding depends upon using these categories
and concepts judiciously, valuing t h e advances they make possible, while at the same time recognizing their limitations.
Hoyle's target article fails on the latter count, because it sadly
neglects the advances in ethology over the last 30 years. The
concepts of the 1940s and early 1950s provided the foundations
on which ethology was initially built, and all honour to the
pioneers who laid them. But the growth of the structure has
required major modifications to those foundations. If neur~~hysiologists
find the concepts of 40 years ago useful, good
luck to them - but let them not write as though ethology had
stood still for 40 years. Such concepts may still have a certain
value ifattention is confined to what Hoyle likes to call "stereotyped, complex, nonlearned, innate behavioral acts," and it may
indeed be wise for the neuroethologist to limit his immediategoals - but ethology itself is not s o confined.
On the descriptive level, it is n o longer useful to make an
absolute distinction between instinctive acts and reflcxes, as
though some types of behaviour were never subject to modifications of threshold, while for all others modifications of threshold
were of primary importance. (Hoyle is actually confused about
his concept of "instinctive act," which he sees as embracing
interactions with other individuals. Interactions have emergent
properties not relevant to an individual's "act.") It is no longer
useful to imply an absolute distinction between activities that
occur "in vacuo" and those that occur as a consequence of
external stimuli. It is also no longer useful to make an absolute
distinction between behaviours that can be labelled as displacement activities and behaviours that occur under the normal
motivational conditions (i.e., between autochthonous and allochthonous activities, to use Tinbergen's terms). It is essential
to recognise that "releasers" may not only release responses,
but also stimulate or guide responses, bring them to an end, and
more. It is indeed "cluaint" and "old-fashioned" to discuss
consummatory acts with the implication that it is their actual
performance, rather than t h e accompanying stimuli, that is
always responsible for bringing behavioural sequences to an
end, though this is convenient for Hoyle in permitting him to
retain, even in 1984, the hydraulic model with its drainingaway
of impulses. Of course, it may be useful to focus on the properties to which these several terms refer when investigating the
neural bases ofparticular instances of behaviour, but it must not
be implied that the distinctions are absolute. In some hut not all
cases, Hoyle does imply this, and yet h e writes as though the
categories were natural ones.
Hoyle wants to perpetuate not only the descriptive categories
of early ethology, but also its explanations. It is surely not
necessary to hark back to the manner in which the "as if'
hydraulic model of Lorenz failed to account for displacement
activities and, as Hoyle describes it, failed to take cognisance of
feedback. Nor should it be necessary to emphasise how the
hydraulic model led to facile implications about neurophysiological mechanisms. In constructing his influential hierarchy of
nervous mechanisms, Tinbergen (1951) simply translated the
reservoirs into nervous centres, and the action specific energy
into motivational impluses. In attempting to account for displacement activities, Bastock, Morris, and Moynihan (1953)
attributed them to "sparking over," thereby translating the
hydraulic energy of the original Lorenz model into electrical
energy with its special properties. Careful reading oftheir paper
shows that it was sometimes nervous or motivational impulses,
sometimes the nervous system o r the behaviour, and sometimes
even the fish that were said to "spark over"! Again, the treatment of the concepts of drive and mood provided by Hoyle
seems almost incredibly naive. Mood, for instance, is defined as
variation in the expression of behaviour, rather than being used
as a concept to explain such variations.
Hoyle also sadly neglects the developlnental issue. He perpetuates the distinction between genetically determined and
learnt behaviour, speaking of the components of a fixed action
pattern as expressions of inherited factors.
Findly, it is necessary to put the record straight concerning
the history of ethology. First, a jibe about von Holst's unfortunately becoming "preoccupied with improving t h e sounds produced by asymmetrical violas" reveals a lack of understanding of
the way von Holst worked; and Huber [q.o. ] who Hoyle implies
took up neurophysiological work "in the last few years especially," has been at it since the fifties. More important, Hoyle
describes Lorenz as Tinbergen's source of inspiration, and
Tinbergen's primary role is reduced to that of "successful
publicizing of ethology." Nothing could b e further from the
truth. Tinbergen was active in research before he met Lorenz. It
is Lorenz who has been the publiciser and Tinbergen the hardheaded scientist. Certainly Tinbergen learned much from
Lorenz, but t h e reverse was also true. Tinbergen took up some
of Lorenz's concepts and refined them o r recognised their
limitations. As their more recent writings show, Lorenz (e.g.,
1981) has sought to retain the 1930-1940conccptual structure of
ethology, while Tinbergen has moved with the progress of the
subject. The result has been differences of emphasis among
ethologists. Lorenz and those influenced by him have continued
to use the hydraulic model, have continued to emphasise the
distinction between "innate" and "learned" behaviour, and
have continued, in discussing the evolution of behaviour, to talk
in terms which imply groudselection. By contrast, Tinbergen
and his followers have come to discuss t h e causation of behaviour in terms more directly amenable to links with neurophysiology; they have endeavoured to understand the develop
ment of behaviour in interactional terms and have kept up with
trends in evolutionary thinking.
Hoyle's paper is to be welcomed in so far as it encourages
work in the field ofneuroethology, hnt it is essential to recognise
that the clear-cut categories and concepts on which he wishes to
base his work, though useful in some contexts perhaps, are not
ubiquitously so.
Neuroethology, according to Hoyle
Franz Huber
Max-Planck-lnstitut lur Verhakensphysiologie, 0-8131 Seewiesen, Federal
Republic of Germany
It was Hoyle's considcrablc achievement to open a new phasc of
quantitative ethology almost 30 years ago, with his electromyographic recordings from freely walking insects. Hc was
also one of the first to succeed in applying the technique of
intracellular recording, long in use with othcr invertel,rates, to
the motoncurons of insects, and was thus one of the founders of
the cellular analysis of insect motor systems.
CommentarylHoyle: Neuroethology
Here, as in some of his earlier essays, Hoyle pleads for a
narrowly defined field (his version of "neuroethology," but a
name such as "field X" or "neuromotor behavior" would perhaps serve as well) in which the participants have nearly or
entirely common goals; thus mutual reinforcement, and hence
progress, might in some sense be optimal. Any civilized means
of promoting cooperation, fruitful concentration, and intellectual self-discipline would seem praiseworthy - how can one
disagree? The results of cooperative work on the locust motor
system are impressive. We await the next great jump forward.
The rub is, of course, that Hoyle chooses to usurp the term
"neuroethology" for his purposes; most of us who think of
ourselves as neuroethologists use the term rather more broadly.
This does not mean that we all descend to the level of Hoyle's
vividly described collectors of "random facts." There are, of
course, mechanisms other than the optimization of designatedfield breadth (which, in practice, o u ~ h to
t be achieved by the
organizers of 'workshops- and symposia) by which wonderful
concentration is brought about. New auestions. and new methods for answering them, arise continually; when any one of these
combines broad interest, challenging complexity, and enticing
tractability, it is the question itself that provides the focus and
motivation for concerted interdisciplinary effort by many workers. The molluscan and stomatogastric work, bird-song production, arthropod motor system, owl hearing, insect movement
perception, bat sonar, fish electroreception, frog hearing, insect
chemoreception, and (dare I say) cricket phonotaxis all come to
mind, among many others. To debate whether each is a cluster
within neuroethology or whether only some subset of them is to
be granted imprimatur under the rubric of "neuroethology"
does not seem helpful to me at this stage ofour adventure. W e
are gaining understanding of interactions among the levels we
are learning to reach, and have little idea now which approaches
will be the cornerstones of more general formulations. Despite
the behavioral significance of "fixed action patterns," surely the
actions of neuroethoIogists cannot be as fixed as Hoyle
Finally, the bit of rhetoric ("unfortunately, this line of progress was finally stilled when von Holst became preoccupied
with improving the sounds produced by asymmetrical violas")
Hoyle uses in referring to the late Erich von Holst's fascinating
experiments on the structural acoustics of stringed instruments
is rather uncharitable. Hoyle also seems not to consider as
"progress" the contributions of this great man to remote brain
stimulation in populations of free birds during his final years of
ill health. One may as well complain in vain that Isaac Newton
spent too much time reorganizing British coinage, or, perhaps,
that Sigmund Freud turned from his early work on crayfish to
other matters.
Vertebrate neuroethology: Doomed from the
David J. lngle
Rowland institute lor Science, Cambridge. Mass. 02142
Hoylc's feisty treatmcnt of issues inherent in ncurocthology is a
useful provocation to rethink long-term goals in this still-burgeoning infant discipline, although h e seems to feel that, for the
sake of a healthy future, the weak sibling, vertebrate neuroethology, should be abandoned in some harsh landscape to
wither away. For those of us whose careers would suffer from
such an outbreak of infanticide, Hoyle's "straight-and-narrow"
sermon forces us to justify our own programs explicitly. This is
ironic for those of us who have already taken a "holicr-thanthou" attitude toward much work in physiological psychology
that appears to have little relationship with the real-life challenges for which brains have evolved. Now, instead ofbasking in
the warm assurance that we alone are studying "real behavior,"
we are asked to explain how we can ever hope to find our way
between sensory and motor domains within the still vaguely
charted core of the vertebrate brain.
Hoyle is quite right in asserting that vertebrate ethology is
overbalanced toward the stud y of sensory systems. There is a
certain pleasure in imagining how objects may be encoded and
represented by animals with strange sensory systems - bats,
electric fish, pit vipers - which at present distracts us from
linking these unique sensory filters with overt behavior. There
is a distinct thrill obtained from recording in the frog's thalamus
single cells that encode the universal auditory characteristics of
"mate" o r astonishment at t h e discovery of "face detector" cells
in the temporal cortex of rhesus monkeys. Most of us are still
working hard to determine the sensory definition of objects and
space, and are not yet ready to connect these "representations"
with useful activities such as movements oremotions. Yet, since
many important connections from sensory systems into limbic
or motor systems are now being adequately defined, it seems
likely that some of us will march on across these borders in the
not-distant future.
Nonetheless, I personally sympathize with Hoyle's insistence
that a focus upon the organization of behavior (the generation of
action patterns and their selection o r modulation by motivational states) should be the core of neuroethology: that is,
looking from the overt morphology of behavior back to the
antecedent eliciting events rather than inward from the sense
organs. Indeed, in the very volume that Hoyle has dismissed as
lacking promise, Adoances in Vertebrate Neuroethology
(Ewert, Capranica & Ingle 1983), I reviewed several new
studies on the interfacing of visual pathways with motor patterns, and concluded that visuomotor output pathways for
consummatory and taxic components of behavior of frogs can b e
distinguished (surely in line with the thinking of the founding
fathers of ethology!).
Progress has also been made in relating the sensory control of
the electric organ discharge of certain fish. The 'j'am~ning
avoidance response" has been elegantly analyzed by Heiligenberg's group (Heiligenberg 1982), using behavioral, anatomical,
and recording methods and always keeping t h e output pattern of
eIectrical signals as the reference point for defining the group's
questions about mediating events. Furthermore, the ability to
uncouple the output of these organs (by curarization) from the
"anticipation" of their sensory effects has enabled Curtis Bell
(1982) to describe three different categories of corollary discharge modifications of electrosensory systems. Hoyle seems to
have overlooked this work of a fellow Oregonian in his implication that useful studies of corollary discharge have not been
undertaken by vertebrate neuroethologists.
Although lower vertebrates (fishes, amphibians, and reptiles)
most clearly exemplify the operation of innate releasing mechanisms and fixed action patterns that characterize old-time ethology, some basicdiscoveries have been made using mammalian
preparations as well. The systematic work of the late john Flynn
(1972) is exemplary in combining anatomical, physiojogical, i n d
behavioral methods in workine out brain ~ a t h w a v srelatine to
the display of aggression in cats. His studies of restrained cats
during hypothalamic stimulation revealed that induction of a
"motivational state shift" would result in "tuning" of certain
visual and tactile reflexes (orienting, biting, or paw-swiping)
that are components of prey-attack. The studies of Donald Pf&
and others (Pfaff, Lewis, Diakow & Keiner 1973) on the fixed
patterns of lordosis in the rat also show that reflexes can be
sensitized by hormone treatmcnt (which perhaps also reflects
activation of a diencephalic tuning system). These insights
might be compared with the discovery by Ewert that preycatching responses of frogs and toads are either inhibited o r
released by modulation of the optic tectuln by the caudal
diencephalon (Ewert, Capranica & Ingle 1983). Recently,
Gerald Schneider (Schneider, Jhaveri, Edwards & So 1984) has
C o ~ n m e n t a r y l H o y l e Neuroethology
shown that predator-avoidance behavior of hamsters is tightly
dependent upon the function of optic tectum (as in the frog) and
little upon the high-level computations of the visual cortex.
Since efferent tectofugal systems are similar among higher and
lower vertebrates, the circuitry underlying avoidance behavior
appears to be a tractable problem in several vertebrate species.
In summary, I submit that Hoyle has ignored some actual
achievements of vertebrate neiiroethology and has underestimated the potential for detailed analysis ofcircuitry defining the
sensorimotor interface in vertebrates (including mammals). Finally, I charge that the fallacy of "invertebrate ethocentrism" is
just as dangerous as the NIH (National Institutes of Health)
practice of mammalocentrism. W e have good reasons to believe
that design features of vertebrate and invertebrate brains are
different in many details. We do not know whether motor
patterning or drive interaction or hormonal facilitation operate
in the same manner within the two universes. While I recognize
that quick breakthroughs in linking sensory and motor mechanisms are the more likely with certain invertebrate preparations, their relevance to an understanding of human perception,
decision making, and action patterns must be validated by
vertebrate neuroethologists who study neural systems with a
more certain resemblance to our own. Some balance between
our dual goals of elegance and relevance must be worked out; I
do not believe that Hoyle has found that balance, despite his
telling arguments concerning the goals of neuroethology.
Table 1 (Kupfermann). Estimate of number of reports of
given organisms reported on at Neuroscience Society
meeting, 1983
- -
Nonhuman primates
Other mammals
Irving Kupferrnann
Center for Neurobiology and Behavior and Deparhnents of Physidogy and
Psychiatty, Columbia Universily Cdlege of Physicians and Surgeons and
New York State Psychiatric Institute, New York, N. Y. 10032
Within a scholarly discussion of neuroethology Graham Hoyle
revives his mischievous and, some might say, malicious argument that his hard and crunchy is better than your soft and
squishy (Hoyle 1976). Hoyle maintains that the amount of
research on Aplysia has somehow obstructed research on truly
interesting arthropod invertebrates, and that the research effort
on Aplysia is not justified by its potential to explain complex
behaviors of the type ethologists are interested in. To gain some
perspective on this thesis, I have tried to obtain a rough estimate
of thk relative proportions of specific organisms currently being
studied bv neurobiolorrists. I analvzed the kevword index of the
abstracts for the last Society for Neuroscience annual meeting.
By also examining a random sample of 100 abstracts, I obtained
an estimate of the proportion of abstracts that did not include a
given organism in the title, which permitted me to adjust the
figures from the keyword index to better reflect the actual
organisms used. The analysis (Table 1) indicates that vertebrates
were used in 88% of the research reports (4,344 out of 4,920).
Rodents (primarily rats) accounted for 51% ofall research, while
nonmammalian vertebrates (one of the central concerns of
ethology) were mentioned in 6% of the abstracts. Invertebrates
accounted for5% of the total (not including 17 reports on olives).
Of the total number of invertebrate papers (Table 2), I estimated
that 38% were on molluscs and 44% were on arthropods. Of
course, these percentages include all types of research, in
neuroethology as well as in other areas of neurobiology. Since
molluscs, compared to arthropods, are more often used for
cellular or biophysical studies, my figures probably underestimate the relative proportion of arthropod studies directly relevant to neuroethology.
i a closely related gastropod molluscs
Reports using ~ ~ l y sand
constitute 92% ofall renorts using.,molluscs. BY contrast, among
the arthropods, no group clearly predominates. Thus, one can
o r unknown
Total estimated reports
They are really complex when you get to
know them
T h e number of organisms reported in the index was multiplied by the adjustment factor to compensate for those titles
that did not cite the organism used. The adjustment factor was
calculated on the basis of inspection of a random sample of 100
abstracts and their titles.
conclude that the arthropods are not being ignored by neurobiologists, although, presumably for various reasons, arthropod researchers have not chosen to concentrate their efforts on
any one type of organism. This diffuseness of effort among
arthropod researchers provides for a broad biological perspective, but may hinder the attempt to solve specific scientific
questions of general interest.
Regarding the assertion that the behavior of Aplysia and
gastropod molluscs is dull and irrelevant to neuroethologists, I
would like to point out that there is substantial evidence that
gastropod molluscs exhibit beautiful examples of complex behaviors. I will cite one set of examples concerning feeding, a
behavior that I am most familiar with (for a sample ofsome of the
work on feeding behavior in Aplysia, see Carefoot, 1967; Jahanparwar, 1972; Kupfermann, 1974; Preston & Lee, 1973; Susswein, Weiss & Kupfermann 1978; and Weiss, Koch, Koester,
Mandelbaum & Kupfermann 1981). Feeding in Aplysia is elicited by highly specific features of their preferred food, seaweed.
The behavior initially consists of an appetitive phase in which
the animal locomotes and searches for food. Direct contact with
food triggers a consummatory response (fixed action pattern)
that consists of a stereotyped sequence of movements that
involve the precise coordination of over a dozen different muscles used in grasping and swallowing the food (Cohen, Weiss &
Kupfermann 1978). Both the appetitive and consummatory
phases occur spontaneously when animals have been fooddeprived for a long period. Feeding in Aplysia is highly dependent upon arousal state, mood, satiety level, learning experiences, and competing behaviors. In short, feeding in Aplysia
(and many other. gastropod molluscs) exhibits virtually every
behavioral phenomenon of interest to ethologists. To varying
degrees, other behaviors ofAplysiaand gastropod molluscs also
CommentarylHoyle: Neuroethology
Table 2 (Kupfermann). Estimate of number of reports of
giuen inuertebrate organisms reported on at Neuroscience
Society meeting, 1983
Other Invertebrates
Total invertebrates
exhibit the complex features that interest ethologists. No
amount of research on molluscs will provide a complete explanation of courtship in ducks; but arthropods will not solve this
problem either. Nevertheless, invertebrates have already provided, and will continue to provide, insights into the neural
mechanisms of general classes of behavior that appear to b e
common among virtually all animals. Hoyle's deriding the
behavioral capacities of a particular group of animals seems
antithetical to the essential features of ethology, namely, understanding, appreciation, and reverence for the true behavioral
capacities of animals.
The squishy revisited: A call for ethological
affirmative action
Janet L. Leonard and Ken Lukowiak
Department of Medical Physiology, Universily of Calgary, Calgary, Alberta
T2N 4N1, Canada
Hoyle emphasizes, quite correctly, that both ethological and
neurophysiological studies on the same behaviors and species
are needed if neuroethology is to prosper. H e argues, however,
that this should be accomplished by restricting neurophysiological attention to a few cthologically respectable specics and
behaviors. The reason for this is hard to understand. The
principles of ethology, as set forth by Lorenz, Tinbergen, and
their disciples, were meant to be generally applicable. It is ture
that ethological studies have emphasized asmall number oftaxa,
but this should not imply that other taxa a r e somehow uninteresting to ethologists. It is much more likely that they simply
have not been studied yet by ethologists. W e need both neurophysiological studies of ethological favorites and, perhaps
more important, ethological studies ofany and all species whose
nervous systems appear particularly accessible to neurobiological study.
Gastropod molluscs, particularly opisthobranches such as
Aplysia, possess what Jonathan Copeland (personal communication) calls the "Cadillac" ofnervous systems. I t is true that these
"Cadillacs" have been used primarily for studies of the cellular
properties of neurons and the control of relatively simple movements. It is unjust, however, to suggest that the animal is
somehow to blame for this. Opisthobranches do not lack behavior: They have lacked ethologists. Over the past two-and-onehalf years we have been working to remedy the situation by
conducting detailed observations of the spontaneous behavior of
Navanax inermis and Aplysia cal$ornica. W e have constructed
ethograms for both species and found that their behavior agrees
quite closely with ethological models and is complex enough to
be interesting in its own right (Leonard & Lukowiak 1982; 1983;
in press a; in preparation). Most opisthobranches are slow
moving relative to insects o r vertebrates. This may be largely
responsible for the idea that they don't do anything. However,
with time-lapse techniques it becomes obvious that they do a
great deal.
Both Nnvanax and Aplysia have respectable repertoires of
FAPs. Our ethograms for N. inermis and A . cal$ornica currently contain 28 and 45 FAPs, respectively. We can expect to
find more as w e look in more detail at juvenile stages and
behavior in the more complex environment of the field. In
particular we have established that in Navannx, normal sexual
behavior involves the active alternation of sexual roles by the
members of a pair during bouts of copulation (Leonard &
Lukowiak 1982; in press b, in preparation). Sexual roles in both
Aplysia and Navanax are behavioral states, and each role involves the execution of a complex series of FAPs. Either species
has tremendous potential for physiological tests of ethological
models, and our results suggest that these opisthobranches may
be ideally suited for the study of male-female conflict with
respect to reproductive strategy, a burning issue in ethology
today. Our observations suggest that opisthobranch behavior is
comparable in complexity to that of insects and other crunchies.
An overview of the scattcred literature on gastropod behavior
reveals instances of male-male competition for mates, parental
care, territory, and everything but eusociality. All animals face
the same challenges from their environment, and being animals
they use behavior to meet them. To bcadaptive, behavior has to
be complex.
Ethology is necessarily a comparative science, and neuroethology must be also. As such, the disciplines cannot afford to
rely on observations from only a small number of "model
systems." For neuroethology to enter a golden age, we need,
not a narrower focus of our attention, but broader training. A
competent neuroethologist must b e au courant with both ethology and neurobiology. It would be foolish for the neurobiology
of the 1980s to pursue the neuronal bases of the ethology of
1950. Hoyle is obviously familiar with the ethological literature,
but his definitions of ethological terms arc quite idiosyncratic
and in no way represent a consensus of current ethological
opinion. In fact, it is highly unlikely that a consensus could be
reached on the definition of such terms as FAP. W e will onlv
have a science of neuroethology when w e have a generation of
scientists trained as such - as neither neurobiologists nor ethologists. In the meantime, we all have to do a lot of reading and
- ---
We are making good progress in the neural
analysis of behaviour
David L. Macmillan
Department of Zoology, University of Melbourne, Parkville, Victoria 3052,
I do think that it is worthwhile for neurobiologists to keep
examining the issues raised in Hoyle's target article. This said, I
find myselfin disagreement with most of its major conclusions. I
will limit my comments to a few of the general principles raised
rather than make specific criticisms of the way the literature has
been interpreted.
Acceptable goals for neuroethologists. At least some of the
goals on the list would be present in the minds of most behavioural neurobiologists. However, as Medawar (1967) has
said, "research is surely the art of the soluble." It is unfair and
inaccurate to imply that the large body ofworkers in this area is
simply on a random fact-gathering spree. The overwhelming
message that I get from reading the introductions to so many
neurobiology papers is that a serious and directed effort is being
made to tackle those parts of the goals that are presently
accessible. When I read the discussions at the end of these
papers, I find that a valiant effort is being made to interpret the
results in a way that will help to bridge the gap between
neurobiology and ethology. This effort largely fails. Unlike the
author of the target article, I d o not feel that this is because the
wrong questions are being asked. I believe this failure reflects a
shortage of basic materials with which to build and bridge.
Aspiring young neurobiologists must see at the outset of their
careers the accolades awaiting anyone who can deal with the
listed goals effectively. The fact that they choose to deal with the
less spectacular but more accessible parts of the underlying
mechanisms means that both they and their supervisors agree
with my position. There are times in science when an extreme
opposing view eventually prevails over a more generally supported one. The fact that we are making sound progress by using
our present approach suggests that this will not be one of those
Who may properly call hlmself a neuroethologlst? There are
two problems with the argument presented in the target article.
First, is there any merit at all in imposing a rigid definition on a
field still in flux? As work progresses a consensus may emerge
concerning the limits of neuroethology, but judgements attempted at this stage are almost certain to b e irrelevant. In the
absence of any true bridge between neural analysis and ethology, intent or rationale forms the only criterion. Second, the
basis of the proposed definition is unsound. No modern ethologist would be sympathetic towards Hoyle's view of the
bounds of ethology or accept the outmoded definitions of fixed
action pattern and other ethological terms (Dewsbury 1978;
Hinde 1982). The discipline of ethology has not remained static
(Hinde 1982) as the target article would suggest. Even if an
attempt to define the field of neuroethology at this time can be
justified, the use of such out-of-date sources to derive the
definition cannot.
Target animals and behaviours. The author has argued on
several recent occasions for concentration ofour efforts on fewer
species (Hoyle 1976), and, indeed, one can make a powerful case
against the haphazard proliferation of experimental animals
simply because a particular animal has not yet been studied.
However, it is also true that many researchers end up asking the
right question of the wrong animal simply 1)ecauseit is available
in the home laboratory, because there is a tradition of using it
there, or because there is pressure to concentrate the field on
selected species. It is entertaining that this author in particular
should now be supporting this position so vigorously, when the
literature abonnds with examples of his equally vehement defense of the opposing view (Hoyle 1967; 1977). H e has argued
cogently in the past that the field of ~nusclephysiology was held
back for years because experi~nentswere confined to "one or
two laboratory animals, especially the frog, and soon, in the way
that men have, 'vergleichende' became almost a word of
contempt among the misguided" (Hoylc 1967, p. 152). There
can be few senior neurobiologists today who could demonstrate
more effectively than Hoyle the productiveness of the comparative approach. Indeed, there can b e few ncurobiologists
who have worked on a greater variety of ani~nalsand few
laboratories that have spawned graduate and postdoctoral research on a wider range of species than his. If one animal or
preparation were demonstrably superior to most others for
behavioural neurobiology, most laboratories would soon focus
upon it. This has happened with locusts and grasshoppers in the
field of neural development The last 20 years of work has shown
that a variety of preparations is necessary. That situation is
unlikely to change suddenly. What Aplysia has told us could not
have been as effectively learned from Shistocercn. What we
have learned about sensory processing from compound eyes
could not have been found by studying cercal input.
In conclusion, I find myself at variance with the tone of the
target article, with the message that progress has been slow
because we have failed to impose guidelines of various sorts
upon our field. I believe that we are making satisfactory progress
and that, in a new field, work will b e concentrated naturally on
those projects and species which prove themselves capable of
yielding the most rapid advancement of our understanding.
I would like to thank David Young for his usual ~vnsidereddiscrission
and for suggestions on this commentary.
Neuroethology: Not losing sight of behaviour
Aubrey Manning
Department of Zoology, University of Edinburgh, Edinburgh EH9 3JT.
Hoyle has been an extremely important figure in the development of neurobiology, and I yield to nobody in my admiration of
his achievements. I also like his direct approach to questions and
his total lack of reticence in expressing his opinions - a nononsense trait that owes a lot to his cultural origins in the North
of England, where spades are called spades and not wrapped up
in the deferential circumlocutions of the South.
I say all this at the outset because, while h e has written a
number of important reviews in this field (e.g., 1964; 1976), this
target article does not number among them. Thereare still some
useful insights to b e found here, but I'm afraid Hoyle's tendency
- often highly productive - to concentrate only on the issues
that h e considers fruitful is here carried to unfruitful extremes.
Hoyle is justified in his criticism of the scope and nature of
much that is called neuroethology. So many people who start
with behauiouralquestions in mind soon drop down through the
levels of analysis to end up juggling with the complexities of
synaptic transmission out of all sight of these questions. Often
they never return. But Hoyle's arguments to encourage a more
behavioural focus are greatly weakened by his idiosyncratic
view of what constitutes "behaviour." At times he seems to
equate it not just with movement but with the movement of
limbs. Hence, he is led to dismiss, or at least underrate, the
importance of Kandel's work (e.g., Kandel 1979) with Aplysia
and Bullock's on electric fish (e.g., Bullock 1977), both ofwhich
endeavours seem to me to embody many of the behavioural and
information-processing virtues that Hoyle calls for elsewhere in
his review.
I am certainly not a neuroethologist and therefore can only
guess how someone working in the field will react to Hoylc's
conception of it. However, it is clear that his view of neuroethology derives from his view of ethology itself. This latter
C o m m e n t a r y l H o y l e : Neuroethology
view I find very strange, for I cannot understand why he chooses
to ignore so much of modem ethological thinking. In keeping
with his obsession with behaviour as movement, h e chooses to
emphasise releasers and the fixed action pattern (FAP) and set
them firmly in the 1950s mould of action specific energy and
I wholly agree that scientists in pursuit of the current fashions
often neglect original basic concepts. In fact, the FAP is indeed a
remarkably robust and useful concept - there is much that
modem ethologists have to say concerning it. But for Hoyle,
"Control offlow of the water in the Lorenz model is the heart of
the matter ofethology."This carries tradition too far! H e quotes
an ethological colleague who tells him that nobody pays much
attention to psychohydraulics now. The reason is that it does not
model behaviour adequately. Hoyle himself recognizes that the
model has its drawbacks, because it lacks feedback control and
also conspicuously fails to account for the patterning of much
aggressive and exploratory behaviour. As ethology has matured,
it has come to recognise that many of the grand old generalisations no longer work. We have to accept, for example, that the
performance of any behaviour may have both incremental and
decremental effects on its subsequent performance. The updated model Hoyle provides may be useful - h e doesn't explain
it enough - but I am uneasy with its grafting of electronic
components onto hydraulic ones. It seems unnecessary, and I
am reminded of the criteria that Deutsch (1960) argued must be
met by behavioural models if they are to b e usef;~.
With reference to the FAP itself, I think that Hoyle's (1964)
ideas concerning "motor" and "sensory tapes" in their control
have been most useful. I d o not understand why h e insists on
making such a clear division between reflexes and FAPs. After
all, the same nervous system is operating and motor patterns are
resulting. Reflexes and FAPs share many properties (some of
which I have tried to illustrate - following Sherrington, 1906,
and Prechtl, 1956) in Chapter 1 of Manning (1979). I agree with
Hoyle that we must assume a large genetic component in the
control of FAP development. They are clear examples of phylogenetic units that it has proved possible for natural selection to
modify in relative isolation from other such genetically programmed units. However, we must admit that our evidence for
genetic control in FAP development is almost all indirect - we
can usually put forward only soft arguments, which are not
based on adequate genetic analysis. Hence, when Hoyle asserts
that, "Most or all of the components of a FAP are expressions of
inherited factors and are subject to the Mendelian laws of
inheritance as wholes," h e is propounding an act of faith, not a
balanced assessment ofthe evidence. I wish it were so simple as
his suggestion that subroutines within FAPs may arise by
mutation. I recommend a careful study of Bentley and Hoy
(1972) to reveal the kind of impasse that we have reached at
Finally, I suppose one of my problems in relating Hoyle's
neuroethology to its mother field is that I don't really have a
clear picture of ethology as a proscribed field ofendeavour. It is
the approach to the behaviour of the whole animal in its whole
environment that represents ethology's great achievement and
has made it so influential. For all my criticisms, I like the way
Hoyle refuses to lose sight of behaviour itself among all the
nerves and muscles.
The ethology of neuroethology
Hubert Markl
Fakultiit fur Biologie. Universitiit Konstanz, 0-7750 Konstanz 1,
Federal Republic of Gennany
Hoyle's contributions to the study of the neural bases of animal
behavior can hardly be overestimated. He himself would seem
to be the last to d o so, as this brilliantly written target article
testifies. In addition to his having made many original investigations and important discoveries on his own, h e has been and
continues to b e a leading pioneer in the methodology of singleneuron work on - more or less - "behaving" animal preparations; and h e has been a continuous source of stimulation for a
large number ofrescarchers in the field described in this article.
A first-hand introduction to how one of the founding fathers of
neirroethology sees its claims and aims is therefore to be welcomed, even if it cannot b e denied that it displays a somewhat
personal, at places even idiosyncratic, view of the matter.
Autobiography (and autohagiography) cannot replace unbiased
historical reprcsentation of a scientific development, even if
written by scholars who have themselves helped to found and
decisively shape this development. To someone who has
watched the impressive advances of the investigations of the
neural mechanisms of animal behavior rather closely, the following reactions suggest themselves: Hoyle's entirely justified
emphasis on the methodological importance of the intracellular
identified neuron approach as a source of progress in neuroethology seems to obscure o r even underrate the immense
conceptual stimulation and encouragement provided for this
field of research by, for example, von Holst's early and admittedly rather crude neurophysiological work on central pattern
generators, o r Roeder's demonstrations that even rather sophisticated-looking natural behaviors of insects are not too complex
to be fruitfully studied at the basic neuronal level; or Bullock's
and his coworkers' success in showing that even in vertebrates
one need only pick a really suitable experimental preparation to
go right down to the neuron level in explaining the mechanisms
behind highly specialized behavior.
Being strongly insect-biased myself, I need not be convinced
that insects are marvelous animals for investigating many basic
physiological and behavioral problems. However, it seems odd
to find this widely accepted fact all but discredited by an almost
group-chauvinist downgrading of research on other (especially
more squishy) phyla. As far as some of the major aims of
neuroethology, as stated by Hoyle, a r e concerned: memory (but
note that h e defines neuroethology first as t h e study of the
neurophysiological events behind innate behavioral acts!), feature detection, motor control, information processing, and development, it is true that work o n the neural circuitry of
invertebrate fixed action patterns can contribute to all of these;
however, to demarcate the field so that neurophysiological work
on fish electrolocation, bird-song control and development, bat
echolocation, amphibian visual or acoustical pattern recognition, o r the ontogeny of cat visual information processing is
either relegated to the periphery o r even expelled seems not
only somewhat arbitrary, but might even turn out to be downright deleterious to the very aims of the field ofneuroethology so
aptly formulated by Hoyle, if his advice were followed to the
word. The same holds true for the study of the endocrine and
especially neuroendocrine mechanisms of behavior: How could
"water-level control" in the Lorenzian motivation model ever
b e fruitfully investigated without clarifying the endocrine effects on the neural machinery as well as elucidating the workings
of this machinery itself? Focusing forces o n those problems that
can at present b e attacked with the highest expectation of
success is certainly an excellent short-term research strategy.
However, in the long run, a field of investigation has to define
itself by the full breadth of t h e phenomena - here of animal
behavior - and not lose in scope what is gained by concentration. Hoyle's view of neuroethology seems to gain exclusivity of
focus by restricting its interests in animal behavior to the most
narrow, and only historically relevant, definition of what ethology is all about. The point of reference should not b e classical
ethology, but the full range of animal behavior.
Altogether, this commendable article also reads to the outsider as strangely possessive and defensive; strangely, because
the Hovle-tvve neuroetholoaical avvroach seems to b e so well
acceptid and-thriving both in the 6 i t e d States and in Europe.
CommentarylHoyle: Neuroethology
Then, why write at such length in battling tones if no one
earnestly denies neuroethology in invertebrates its ranking
place in modern biology? I can only understand this as a
particularly nice demonstration of human ethology in science.
The article seems an effort to rally the tribe, to stake out its
territorial claims in order to monopolize its resources, to define
the defended boundaries against intruders (and defectors), to
affirm precedence of occupation, to throw out foreigners or to
relegate them to lower services, to give its members a feeling of
historical identity by deriving their unifying tribal goals from the
gospel of sanctified, Nobel-pized founders, to erect common
linguistic and conceptual totem poles for the society of friends,
and, finally, to christen the true believers through the psychohydraulic flush toilet handed down to the British Society of
Experimental Biology in 1949! And why all this? Now, economic
sociobiology may not be beneath even the most high-spirited
endeavors of the human mind! The last sentence gives it all
away: "May granting agencies see the ultimate wisdom of
supporting the endeavor." Optimal foraging in the world of
academia, the ethology of neuroethology. Which is not to say
that I would not fully agree with this videant consules message of
Professor Hoyle.
Resurrecting Lorenz's hydraulic model:
Phlogiston explained by quantum mechanics
Zodogisches lnstitut der Universitat, 4051-Basel, Switzerland
Sciences during their development pass through necessary
stages of oversimplification, of elementary models and catchy
concepts. As understanding proceeds, more and more qualifications are introduced; the appealing clarity of the original concepts is obscured and is replaced by a more accurate but more
tedious description. Ultimately, the original concepts drop out
of use, and with luck are superseded by a new formulation at a
deeper level of analysis. Within the field, the original concept is
at best relegated to a useful shorthand in communication among
practising scientists who understand its problems, but outside
the field, it often remains long enshrined in the works of
popularisers and in the thought processes of scientists in other
areas. Examples abound, from phlogiston to Newtonian physics, in the homunculus and in Mendelian genetics, in the
ethological terminology of the 1950s and (to cite a tiny example
from our own field) in the command neuron. [See Kupfermann
& Weiss: "The Command Neuron Concept" BBS l(1) 1978.1
My first major criticism of Hoyle's article is that it resurrects a
simplified parody of the ethology of the 1950s, claims it represents the real behaviour of animals, and holds u p this illusory
construct as a desirable target for modern neurobiology. H e
proposes, in short, to explain phlogiston with quantum mechanics. An outsider to behavioural science and imprinted upon the
ethological concepts ofhis youth, he takes some of these (though
ignoring others, such as ritualisation and intention movements,
which fit less readily into his scheme) and elevates them to a
peak ofreification barely contemplated even by their originators
35 years ago. He dismisses offhand the careful work of two
subsequent generations of ethologists who have revealed the
limitations and evaluated the uses of this terminology and ofthe
Lorenzian hydraulic model, and, incredibly, whecls the latter
back on stage. This mummy, dusted and superficially decorated
with nei~rophysiologicalterms and with the difficult parts concealed in labels such as "computer" and "comparator," is to be
investigated through modern circuit analysis.
I cannot believe that this would be afruitful approach. True, it
would indced b e nice to have a unifying theory of neurobiology
to "explain" the profusion of alternative designs, but this one
will not do it. Natural theologians collected natural history and
life history data for 300 years before the Darwinian theory of
evolution rationaliscd thc hopeless diversity, and that theory
would not have originated in satisfactory form had it not been for
their labours. Patience, neurobiology - better no theory than a
retrograde one, one which has already delivered its contribution.
For it is simply not true that neurobiology and ethology have
not previously met, and this is my second major criticism ofthe
target article. Hoyle grossly understates the extent to which
neural circuit analysis has already provided a basis for the
understanding in neural terms of those aspects of behaviour
which "interested the founders of ethology." T o give one example: There are some behavioural components well described as
"fixed action patterns" in the original sense, and there are some
neurons that fit t h e original concept of "command fibre." For 38
years we have known that one command fibre and its associated
postsynaptic circuitry is the basis of one FAP - Kees Wiersma's
brilliant work (1947) on the crayfish lateral giant fibre made this
clear and established him as the authentic founder of the sort of
neuroethology Hoyle advocates. By the time the ethologists
were working the same conceptual ground 10 to 20 years later, it
was already clear to Wiersma and to other pioneers of the neural
basis of instinctive behaviour, such as Roeder, that much behaviour is not organised in this way, even in crayfishes or moths.
In this area, neurobiology had preceded ethology: In others, the
corresponding neural investigations have been made subsequently, as the necessary techniques and self-confidence
An outstanding feature of Hoyle's target article is the number
of highly relevant neurophysiological studies he ignores. We
have, for example, detailed studies at the synaptic level of how
stimulus filtration is achieved in both insects and vertebrates,
especially within the visual system (e.g. Barlow & Levick 1965;
Hubel & Wiesel 1974; Rowell, O'Shea & Williams 1977, among
many others). W e understand in many preparations the activation of complex circuits by key stimuli of external origin, circuits
producing either episodic or cyclically repeated behaviour; e.g.
the release of the various tailflips or alternatively ofswimming in
the crayfish (reviewed by Wine and Krasne 1982) o r of escape
swimming in Tritonia (Getting 1976; Lennard, Getting& Hume
1980). Some of t h e longest coherent sequences of fixed action
patterns known, the moulting programmes of arthropods, have
been analysed in depth in moths (e.g. Truman 1979), locusts
(Hughes 1980), and crickcts (Carlson 1977): T h e release of this
behaviour through key stimuli of internal origin (hormonal
secretion) is being actively investigated (e.g. Truman, Mumby
& Welch 1980), as is the comparable release of the egg-laying
behaviour of the scahare (reviewed by Scheller, Rothman &
Mayeri 1983). W e have descriptions of identified intraganglionic interneurons in locusts which each drive discrete but
overlapping assemblages of motor neurons, producing elemental complex movelnents (Burrows 1980), a phenomenon which
would surely have delighted Tinbergen in 1950. Particularly
puzzling is Hoyle's distaste for the st~matogastricpeparatioi,
a ~ ~ a r e n t due
l y to the fact that the movements of the lobster
stomach were not described by Lorenz. I n my laboratory, we
are currently investigating the circuits that allow a flying locust,
equipped with a relatively rigid central pattern generator for
flight and associated sensory feedback, to integrate exteroceptive information with this mechanism and make adaptivecorrections to the flight path, or steer at will towards or away from
objects (reviewed by Reichert, in press). I am not sure that this
work would qualify for Hoyle's brand of neuroethology (though
if locust jumps and seaslug swims do, surely locust flight is
allowed in); but if it does, then it is piquant that the most useful
source of comparative information for our analysis is certainly the stomatogastric preparation.
In the space allowed it is impossible to rise to all of Hoyle's
deliberate o r unintentional provocations. I think it should be
mentioned, however, that his article may give a false impression
C o m m e n t a r y l H o y l e : Neuroethology
that ethology stagnated without fertilising a new and active
interdisciplinary science. Nothing could be further from the
truth. The great achievement of classical ethology was to make
biologists realise to what a huge extent behaviour, even the
complicated behaviour of the higher vertebrates, is based on
species- (or other taxon-) specific genetic instructions, and, so
based, is directly subject to classical selection. Ethology may not
have revolutionised neurobiology (though the interaction was
certainly more fruitful than Hoyle appears to realise), but it was
instrumental in causing the present-day fusion of behaviour,
ecology, population genetics, molecular biology, and evolutionary biology that has become probably the most exciting area of
biology since Darwin. Whole new fields of investigation (e.g.,
sociobiology, optimal foraging strategy theory, and so on) have
arisen as the direct consequence of this fusion. The Nobel prizes
to the ethologists were certainly appropriately awarded. It is
likely to be a long time before neurobiology makes advances as
Points of congruence between ethology
and neuroscience
Wolfgang M. Schleidt
Depament of Zoology, Univemiiy of Maryland,
Cdlege Park, Md. 20742
Let us assume that ethology is the subdiscipline of biology that
deals with the behavior of organisms (following the proposal of
Lorenz, 1981), and that neuroethology is the subdiscipline of
biology that deals with the sensory, neural, muscular, and
glandular substrata of behavior (following the intent of Hoyle's
target article). Even though any one behavior is supported by a
specific substrate, behavior and substrate can be investigated
independently, at least in principle, and either investigation has
l come U D with its own ex~lanations.We will not
the ~ o t e n t i ato
seek to explain behavior by its underlying structure, as attempted by ontological reductionists, even though we may find
indications that the underlying structures set specific limitations
on the range of potential behaviors. However, we do accept the
conclusion that only the overt behaviors and structures are
directly subject to natural selection, and that any substrate
within the organism can b e reached by natural selection only
through the surface (Schleidt 1981). Accordingly, we must not
ignore the close correspondence between overt behavior and its
internaI substrate, and must deal with it, not as ethologists or
neuroscientists, but as biologists.
In my view, the essence of a scientific explanation is to
provide some kind of map that shows the relevant objects and
their features while omitting irrelevant clutter. "To explain
something" means, literally, to lay it out flat, so that it becomes
obvious and nothing remains hidden. Any particular scientific
topic can be represented not only by its topographic map, but
also by one of the traditional forms of scientific description, such
as veibal explanations, working models, or sets ofaequations.
Each form of description has advantages and disadvantages.
Transparency, eloquence, and ability to minimize redundant
information and noise vary, but ultimately, all forms are mutually translatable. The idea of a "map," and correspondingly, the
idea of scientific investigation as a "mapping process," has the
advantage of representing the attempted congruence between
"the real world" and the selected "scientific topic." Thus,
whenever congruence is absent we are alerted to the fact that
our attempted explanation has failed. In order to clarify the
relation between ethology and neuroethology, I want to point to
two kinds of inappropriate explanations: The first corresponds to
the use of the wrong map, comparable to the attempt to navigate
the streets of Vienna with a street map ofwashington, D.C. The
second is equivalent to the use of a map on which the con-
gruence is coincidental o r only partial, as in using the storm
sewer system map when a street map is needed.
In comparing the scope of ethology with that of neuroethology
the problem ofcongruence is most important, since both types
of erroneous application of "maps" have created confusion in
both fields, and have raised false hopes and expectations. We
tend to ignore basic behavioral and structural differences among
members of different animal phyla, and we confuse relations
among behavioral elements with relations among anatomical
structures that we suspect are important for behaving.
First, we have to remind ourselves that the basic theoretical
framework of ethology, including the concept of the fixed action
pattern (FAP), was conceived mainly from studies of vertebrates, mainly birds and mammals. T o this date, no fine-grained
comparison of different taxa exists that allows us to decide
whether or to what extent the particular features emphasized as
significant in birds (e.g., Lorenz 1932; 1970) are also significant
in other classes, such as hydrozoans, crustaceans, snails, or
cyclostomes. In fact, until recently, even a format for finegrained descriptions of behavior that could make such a comparison feasible was lacking (e.g., Drummond 1981; Finley,
Ireton, Schleidt & Thompson 1983; Schleidt & Crawley 1980).
However, some differences in the behavior of the members of
different taxa are too obvious to be ignored. For instance, birds
and mammals show a wide variety of adaptive modifications of
behavior (Lorenz 1965) that are blatantly absent in insects. This
difference in learning ability may well indicate a fundamental
difference in the overall organijration of behavior in these taxa.
The differences in anatomical structure are too obvious to
require any further emphasis. Thus, t h e assumption that a
better understanding of insect behavior will help us understand
human behavior is unfounded, except for the very general fact
that we understand principles by comparing different items
such as systems or organisms. Or, more aggressively phrased: If
we want to understand human behavior, w e should focus on the
study ofother primates, and possibly other vertebrates. But the
greater the genetic distance, the less immediate will be the
applicability of the results to the human case.
Second, w e must not forget that the original prototypes of the
FAP are the grunt-whistle of t h e mallard and t h e fly-catching of
the starling (and, unofficially, the sexual act ofthe human male).
The patterns of locomotion in fish, worms, and centipedes were
added with the physiological explanation for their spontaneity in
mind (von Holst 1939; Lorenz 1937). The "flush toilet model"of
the FAP (Lorenz 1950) was introduced as a chaIlenge to the
persistence of Pavlovian-Sherringtonian thinking in terms of
reflexes, and as a logical alternative to the Cartesian idea of
stimulus control. The model emphasized the internal production of excitation, and showed how internal and external control
could b e integrated, with the method of "dual quantification"
(Lorenz 1943) in mind. However, it was certainly not intended
as a hypothetical blueprint for a particular neural subsystem. It
was inspired mainly by the inventor's intimate knowledge of the
anatomy and physiology of both the motorcycle, including its
carburetor, and the human body, including its urogenital tract,
but not especially by his knowledge of brain anatomy (documented in Lorenz 1936). This is not mere inferenceon my part,
but an authentic statement in the sense that I was privileged to
assist Konrad Lorenz in designing the first drafts of the model
and executing it in pen and ink.
I believe that progress in our understanding of the FAP and
the implications of its model can b e made by correcting erroneous assumptions (e.g., Lorenz 1981, p. 181, Fig. 1%); by
analyzing the model's assumption in greater detail and mapping
it onto a different frame of reference (Figure 1);and by checking
the features against those of a particular animal's behavior (e.g.,
Schleidt 1964; 1965; 1974). But to elaborate on the fine details of
the old "psychohydraulic model" and to represent a particular
function by combining a variety of elcctronik, hydraulic, and
logic symbols (e.g., Hoyle's Figure 4) is confusing. Although the
Cornmentaryl Hoyle: Neuroethology
generator of
integrator and
Figure 1.
(Schleidt) Functional diagram of the "psychohydraulic model" (Lorenz 1950), according to Hassenstein (1983).
1984 model fails to explain the behavior any better than did the
original 1950 version, it leaves me in a state of awe about the
hypothetical neural structures and functions, and evokes visions
of Rube Goldberg's creations (Marzio 1973).
The ethologist's conceptual map of the FAP could conceivably
be as different from the map envisioned by the neuroscientist as
the street map of Vienna is from the map of its sewers. Navigating the streets of any city with the help of its sewer map or
navigating the sewers with the help of the street map would be
equally confusing, in spite of the obvious partial congruence
between the two maps. Ultimately, we must widen our scope
and think as biologists. We need to have available and use both
maps with equal skill in order to make a novel contribution to
our understanding of the neural underpinnings of ethology. This
is not just a matter of finding the neural mechanisms that
support behavior, but locating among all the clutter the particular points of congruence.
Neuroethology - how exclusive a club?
Allen I. Selverston
Department of Biology, University of California, San Diego,
La Jolla, Calif. 92093
For anyone who has been acquainted with Professor Hoyle over
the past 20 years, the argument that insects are the only
salvation for neuroethology is not entirely new. Indeed, he has
spread this view at every opportunity, and my initial response to
this particular effort was that there is very little new here. But,
in fact, I think it can be said that neuroethology is at some kind of
crossroads in its development, and an examination of future
progress in this relatively new discipline might be worthwhile.
For me, the application of rigorous neurophysiological tcchniques to ethology has always been a natural progression toward
understanding the fundamental determinants of behavior.
Since there are interesting behaviors in all phyla, and a mechanistic explanation of them would provide the basis for testing the
principles that have emerged from purely ethological studies, I
have never felt the need to restrict the field to a few especially
favored organisms. But if we are to apply the techniques of
neurophysiology, then the animals selected and the behaviors
scrutinized have to be experimentally tractable. Ifwe accept the
recommendations in Moyle's target article, it is only insects that
have both really interesting behaviors and nervous systems that
will yield to the microelectrode. In a marvelous exposition of
biased, confused, and contradictory thought, Hoyle rejects
most other preparations, including many that have added to our
knowledge of neuroethology. Aplysia is treated with contempt,
while a close kin, Tritonin, is held up as thc only animal that has
come close to providing us with a complete explanation for a
fixed action pattern. Are we to believe that only preparations
with which Hoyle has been associated a r e worthy of study?
Hoyle has, ofcourse, alsolabored mightily and for many years
on insects, but where is the progress? Has h e produced a
neurophysiological explanation for locust marching, a project he
began over 30 years ago? To b e fair, this explanation is still
missing . . . and why?
The neuroethological approach I was taught as a graduate
student was to first study the behavior quantitatively, making
ethograms and the rest. Then one examined the muscles and the
neuromuscular apparatus so as to establish a transfer function
between the nervous system and the movements. Pkrticularly
useful was recording from the muscles, while the behavior was
occurring and then correlating this information with films of the
movements or outputs of movement detectors. This was about
all one could d o with what were essentially noninvasive techniques, and for many today, such methodology remains the end
point for the physiological analysis of an ethological problem.
Further progress required a semi-intact or isolated CNS preparation in order to work out the circuitry and the mechanisms
underlying the movements, and when this was achieved, to try
and relate it all to the behaving animal. It was at this point that
the two mutually contradictory features of neuroethology became apparent. The animals with the ethologically most obvious
and complex behaviors had the most difficult nervous systems to
work on experimentally, and those animals with large, easily
accessible neurons were, indeed, usually less interesting from
an ethological point ofview (but only for those investigators who
were shortsighted). Hoyle's prescription for reconciling these
opposing truths seems, at first glance, to be entirely reasonable.
His primary target for aspiring neuroethologists would b e a
description of motor neuronal circuits and the role of proprioceptive feedback in shaping the final motor programs. H e
would also like to know how they are turned on and off and
controlled at a cellular level. But what are the requiremnts for
the attainment of these worthy goals, and how do insects in
particular measure up?
1. All of the motor neurons have to be identified. Not too
hard, thanks to the development of backfilling techniques.
2. All of the premotor interneurons involved in generating
the behavior must be located. Extremely difficult. They are
small, numerous, and the cells must be penetrated and held
while the behavior is in progress. Furthermore, it must be
shown that perturbing their activity has an effect on the motor
output program.
3. All of the ephaptic and synaptic connections behveen the
interneurons themselves and between the interneurons and the
motor neurons must be identified and characterized in terrns of
their effectiveness and temporal properties. In addition, they
must be rigorously proven to b e monosynaptic.
These last two requirements have usually become the Waterloo of insect neurophysiologists, even if they have survived the
CommentarylHoyle: Neuroethology
battle offinding all the cells involved. The main reason is that, in
order to obtain the necessary data, dual penetrations must h e
made between pre- and postsynaptic neurons that have been
previously identified. There are only a few laboratories in the
world able to perform this feat routinely (and unfortunately
Hoyle's is not one of them). There are two more requirements:
4. The neuronal and hormonal inputs to the pattern generating circuits must b e located and characterized.
The inputs play a key role in interfacing the circuits to the
environment, even in the case of fixed action patterns. For
insects, many workers feel that some of the proprioceptive
pathways may actually be p u t of the motor pattern generator.
Because such inputs can easily b e manipulated experimentally
(being peripherally located), they are easier to deal with than
premotor interneurons - the CNS largely remains a black box.
5. Finally, knowing all of the cells and circuits involved, it is
still necessary todetermine the algorhithms that are used by the
circuit in the production of behavior. This usually means the
formulation of an experimentally testable hypothesis, and this
can be even more difficult that unraveling the circuit.
While these practical problems might not be of interest to a
deep thinker, the goals Hoyle hopes to achieve will be difficult
to attain without considering them realistically, and this he has
failed to do.
The example given in the target article, concerning the locust
jump circuit, is among the best examples ofwhat is possible with
insects, but it should be pointed out that this is a relatively
simple behavior compared with courtship and mating, for example, that all of the neurons and synapses involved have still not
been identified, and that a description of how this circuit
actually worksis not available. A circuit is anecessary start - but
it alone is not sufficient to explain a behavior.
If the complex circuits of insects are so refractive to thorough
electrophysiological analysis, can the circuits of other invertebrates with less wonderful behaviors be of value to neuroethologists? Even if, by Hoyle's definition, some researchers
are restricted from admission into the neuroethology club, I
think the elucidation of how many motor circuits work might b e
at least of academic interest to some comparative neurobiologists. It will certainly be of value to vertebrate physiologists as
model systems.
The motor patterns produced by the lobster stomatogastric
ganglion drive the teeth and because the movements (unlike
limbs) cannot be seen, Hoyle feels their study lies outside the
scope of neuroethology. However, the neuromuscular apparatus and the observed motor patterns are in fact precisely identical
to the systems and the behaviors that he has formally blessed.
There is no a priori reason to think that the mechanisms
underlying such varied motor patterns as snail feeding, leech
heartbeat or Tritonia swimming may not share features common
to cyclic motor patterns in insects. Evolution is probably more
conservative than Hoyle would have us believe.
Then, what is the future of neuroethology, and who should
bring this field to new shores? The discipline may constrict its
horizons to meet Hoyle's restrictive requirements. I hope that it
does not. I think its future lies not in exclusion but in diversity. I
am seriously concerned that, without the insights gained from a
wide spectrum of preparations that combine the best features of
interesting and complex behaviors with experimental tractability, neuroethology may become a discipline which will not
only have been born but will also have died in our lifetime.
Keep the scope of neuroethology broad
James A. Simmons
Institute of Neuroscience, University of Oregon. Eugene, Oreg. 97403
The contributions of ethology to our understanding of the
mechanisms of behavior are considerable, and it rightly belongs
among the disciplines that constitute the ncuroscic~lces.It can
b e distinguished from psychological approaches to behavior in
general terms by its strong insistence upon studying the natural
behaviors of animals in their normal environments. This reveals
a more direct concern with evolution than is characteristic of
psychology. Comparative psychology has at various times in its
history professed to do the same, but it has frequently failed to
work comfortably with either a broad spectrum of species or a
biologically sound selection of behaviors to study. It has, however, participated in the long and rich conceptual development of
psycholo&, which surpasses a narrowly defined ethology in the
so~histicationof its theoretical constructs. Verhaltensahusiolo. "
gie, which is distinguished from comparative psychology by
being truly comparative and concerned with natural behavior,
has converged upon psychology in its theoretical constructs.
This process of convergence has procecded so far that the study
of some topics, such as song learning in birds, requires the
language of cognitive psychology to express some of its ideas.
In his article on the scope of neuroethology, my colleague,
Professor Hoyle, argues that neuroethology should take a relatively narrow, although certainly highly focused, definition of
itself. It is true that ethology can be distinguished from psychological approaches to behavior in specific terms by its concept of
the fixed action pattern as the most basic, biologically relevant
element of behavior. Because the fixed action pattern is a
functional unit, representing an adaptive behavior that has
emerged genetically and been sha p ed in evolutionary processes, it is a key concept for uniting understanding of internal
and external causes of behavior. This concept is a significant
achievement and represents an enduring contribution to the
ideas of neurosciences. And, surely, no one can fault the assertion that one ought to study an organisms's natural behaviors
evoked under natural conditions.
The definition of neuroethology as the study of the neural
mechanisms underlying the behaviors that constitute the science of ethology is also quite reasonable. The subject matter of
ethology is, therefore, the issue at hand in attempting to delineate neuroethology from other components ofthe neurosciences.
These points are nicely made by Hoyle in his target article. The
article seems, however, self-defeating in its attempt to chart a
future course for neuroethologists. The source of this difficulty
appears to be the inconsistency between a narrow and rcstrictive identification of the subject matter of ethology and a
broad and advanced identification of its goals.
For example, it is argued that current research on the nerrral
mechanisms of bird song, visual pattern recognition in fish,
visual orientation to prey in toads, and echolocation in bats
really represent Verhaltensphyswlogie rather than neuroethology. The study of jumping and flying in grasshoppers is ncuroethology, however. The approach, which has worked so well
in determining how the nervous system of a locust controls
walking or flying, consists of specifying at each stage (or cell) in
the process exactly what happens during execution of the fixed
action pattern. This amounts to measuring the transfer functions
of the components and integrating them to then describe how
the system they compose actually works. This is entirely appropriate, but it is unlike the practices ofscientists who have so far
contributed the most to developing theories of information
processing in the nervous system. Such theories have emerged
most frequently from the study of higher-order behavioral
phenomena and have represented an attempt to extract some
principles of brain function from sophisticated rclationships
between stimuli and responses.
The most interesting models of information processinn in the
brain come primarily f&m psychology, where the most sbphisticated stimulus-res~onse relationshins have historicallv been
the eiectric-field model'of the
addressed. ~ x a m ~ i include
brain, which emerged from Gestalt psychology; the sensoryquality models specific to vision and hearing which emerged
from psychophysics; and the extraordinary theory of Hebb
CommentnrylHoyle: Neuroethology
(1949), which emerged from a variety of psychological themes,
including the work of Lashley (1929), the observations of clinical
neurophysiology, and research on perceptual development.
These theories all result from taking the intellectual risks that
are a big part of the business ofscience - attempting to describe
the mechanisms underlying phenomena before it becomes technically feasible to think of describing these mechanisms from
direct, unambiguoiis measurements. Great though the achievements of modem neuroscientists may be in measuring such
things as the response properties of sensory neurons and piecing
together the neural representation of stimulus features, the
concepts corres p ondin g to feature detection and stimulus processing may have been more difficult to come by in the beginning, when they were deduced from psychophysical data.
Which is the greater intellectual step: discovering that the
properties of perception require the brain to exhibit interactive
properties such as can be modeled as electric fields, or carrying
out very difficult measurements to demonstrate such interactions in neural responses? I do not know the answer to this kind
of question.
I think that it is preferable to live with the manifest plurality of
interests within, and overlap among, the disciplines that study
behavior and the nervous system. It may be less tidy than being
able to specify without ambiguity the content of ethology,
comparative psychology, and Verhaltensphysiologie. It is true
that working out the neural mechanisms of-behavior will demand discipline and dedication to the task, but these qualities
are not absent from what has already been done. The kinds of
ideas driving ethology, psychology, and Verhaltensphyswlogie
are too similar, and the concepts these disciplines create are too
much alike to consider them as parallel and independent
As a footnote to the proposed exclusion of research on echolocation in bats from neuroethology, I am reliably informed that
Karl von Frisch once expressed regret that he had not discovered and studied it.
The proper domain of neuroethology
Horst D. Steklis
Department of Anthropology, Douglass Cdlege, Rutgers University,
New Brunswick, N.J. 08903
I am in agreement with Hoyle's general sentiments about the
present standing and future prospects of neuroethology. I; too,
have been puzzled by the liberal (mis)application of the term
"neuroethology" to seemingly random (from an ethologist's
viewpoint) pieces of neuro- or behavioral physiology, and I am
disappointed by how relatively little attention is given (especially in higher vertebrates) to the neural bases of FAPs and
related phenomena. I suspect that a major reason for this
inattention to ethological concepts as theoretical guides in
physiological work is that concepts like the FAP have largely
fallen into disrepute (especially in America) as useful explanatory constructs for the behavior of higher vertebrates (e.g., primates). (Witness the heated reaction to sociobiology in America!) Along with Hoyle, I maintain that such concepts are
appropriate in the neurophysiological analysis of complex behaviors in all vertebrate orders, including primates, and I will
provide some relevant examples from areas that Hoyle, unfortunately, considers as lying outside the proper domain of neuroethology.
Hoyle draws the boundaries of the discipline rather sharply,
dismissing in a few sentences the entire fields of development,
neuroendocrinology, and neuropharmacology as not having any
valid intellectual subdivisional status. It seems to me that
neuroethology overlaps significantly with all of these fields
insofar as they contain specialists interested in understanding
"the generation of particular kinds of complex behavior. "There
has been a thrust in recent years to elucidate the neuraldevelopmental bases of species-typical behaviors (including
such phenomena as imprinting) in avariety ofvertebrate species
(e.g., Gottlieb 1973; 1976). This work has proved extremely
valuable in clarifying the role of experience in the development
of species-typical behaviors. Admittedly, this work has not (to
my knowledge) led to the identification of neural circuitry
responsible for the execution of FAPs, but it should nonetheless
be encouraged, as it will continue to bring improved clarity to
these widely used and much misunderstood key ethological
One particular area of neuroembryology that holds much
promise for contributing to neuroethology is fetal neurosurgery.
The work by Taub (1977) stands as a particularly compelling
demonstration of the existence of FAPs (or something very close
to them) in a higher primate species: Complete unilateral
forelimb deafferentation (by dorsal rhizotomy) in fetal rhesus
monkeys at the end of the second trimester does not impair use
of the deafferented limb in t h e complex, coordinated movements of ambulation and reaching at 3 to 5 months of age.
Similarly, bilateral forelimb deafferentation at birth leaves intact spontaneous motor responses like walking, running, climbing, and reaching, even after blindfolding. These data strongly
suggest that motor programs may be "hardwired" into the
primate CNS before birth. Without this type of developmental
analysis, however, there would be no point in exploring the
primate brain for the location of innate motor programs for
complex behavior.
Certain work by reproductive neuroendocrinologists (much
of which includes neuropharmacology) also fully qualifies as
neuroethology (in the sense defined by Hoyle). What springs to
mind is work on the role of gonadal hormones in motivation and
sensory-motor function. PfaKs recent monograph (1980) details
the neural circuitry snd hormonal basis of t h e female rat's
lordosis response and makes explicit how this behavior pattern
fits the classic ethological model of FAP, IRM, and (some will
shudder) even Lorenz's hydraulic model of motivation. In brief,
the lordosis response of the estrous rat has all the features of the
classic FAP, being highly stereotyped, species-typical in form,
and released by highly specific stimuli (i. e., localized cutaneous
pressure). The release of this pattern is dependent upon the
action of estrogen (which is the motivational variable) o n specific
hypothalamic nuclei, which in turn provide a descending influence on brainstem and spinal cord such that in the presence of
cutaneous pressure on the female's posterior, lordosis behavior
will occur.
I think this neuroendocrinological approach to the physiological basis of motivation underlying species-typical behavior
patterns holds great promise also for species with complex
nervous systems, including primates. Aspects of the neuroendocrine system (e.g., steroid uptake sites) and neurochemical
projection systems show substantial conservatism among the
major groups ofvertebrates, which may indicate commonalities
in the physiological mechanisms of motivation. The estrogen
facilitation of central neuronal responsiveness to regional cutaneous pressure described by Pfaff(1980) for the female rat has,
for example, also been described for female squirrel monkeys,
who like the rat (but unlike higher primates) have sharply
circumscribed estrous cycles (Rose (Ir Michael 1978).
The specific motor and sensory effects produced by electrical
stimulation of the cat hypothalamus o r midbrain in the context of
predatory attack (Flynn, Vanegas, Foote 81Edwards 1970, for
review), appear fundamentally similar to t h e steroidal influence
on neural tissue described above. Stimulation facilitates local
reflexes (e.g., head orientation, biting, pawing) that are incorporated into the species-typical predatory motor pattern. A type of
sensory biasing appears to be responsible, so that, under brain
stimulation, visual field responsiveness to moving objects is
enhanced - Flynn e t al. (1970) suggest this is mediated by direct
hypothalamic influence on visual cortex cell activity - and
CommentarylHoyle: Neuroethology
peripheral sensory fields are enlarged, making tactile stimuli
applied to the muzzle, for example, effective in eliciting head
orientation and mouth opening. Such changes in sensitivity to
sensory stimuli can also be produced by amygdaloid stimulation
(Block, Siege1 & Edinger 1980): Depending on electrode location, sensory fields of the cat's lip can be either expanded or
constricted and attack facilitated or suppressed, respectively.
Finally, gonadal steroids have I ~ e e nshown to affect brain stimulation - elicited attack behavior in both cats (Inselman-Ternkin
& Flynn 1973) and rhesus monkeys (Perachio 1978). It seems
entirely appropriate that one of the earlier uses of the term
"neuroethology" was by two Swiss investigators in describing
their work on brain stimulation - evoked attack in the cat
(Brown & Hunsperger 1963).
Since gonadal hormones have been shown to have significant
effects on the processingofstimuli by the CNS in both man and
other animals (Gandelman 1983, for review), it seems probable
that some of the physiological mechanisms of motivation described above are common to man and other animals. It is
conceivable, for example, that basic emotions selectively bias
attention toward salient sensory stimuli, such that the latter
serve to "release" prepotent motor responses. Furthermore,
such sensory biasing mechanisms could have an evolved basis
(or innate components, as is likely in the decoding of primate
facial expression, Sackett, 1966), and hence be proper targets for
ethological study.
Substantial progress has been made in recent years in elucidating the neural bases of (visual) attention mechanisms in the
primate brain (e.g., Lynch 1980), including the demonstration
of direct hypothalamic connections with neocortical sensory
areas (Mesulam, Mufson, Levey & Wainer 1983); and proposals
have been made about the role of opiatergic systems in sensory
stimulus filtering (Lewis, Mishkin, Bragin, Brown, Pert & Pert
1981). All of these findings have direct relevance for a neuroethology of large-brained mammals, but I suspect that it will
take some convincing for neuroscientists to accept traditional
ethological concepts as appropriate for the analysis of higher
mammalian behavior patterns.
Ethology and neuroethology: Easy
accessibility has been and still is important
Edgar T. Walters
Department of Physiology and Cell Biology, UnivemiIy of Texas Medical
School, Houston, Texas 77225
Hoyle has presented a clear and interesting vision of neuroethology. Several of his.assumptions, however, undermine
the ambitious program for "budding neuroethologists" that h e
lays out. Particularly troublesome is the assutnption that only
those categories of behavior and those species that have been
studied by the classical ethologists are worthy ofneuroethological analysis. This assumption is combined with a hasty dismissal
of the large amount of work on Aplysia, which "has been
dictated solely by the easy accessibility of its . . . cells." I think
there is an interesting irony here. It is true that the Aplysirr
nervous system permits extensive access to various identified
neurons with well-defined functions, and that this easy access
has encouraged the neurobiological study ofAplysia. Although I
am not an ethologist, it seems to me that easy accessibility was as
important for the classical ethologists in their selection of species and behaviors for study as it has been for c c l l ~ ~ l aneur
robiologists. The ethologists have been primarily interested in
incorporating behavior into the framework ofzoology and evolutionary biology (e.g., Lorenz 1950; Manning 1972; Tinbergen
1951). I submit that they selected species and behaviors for
study, not because each was "of sufficient complexity to excite . . . serious interest," or "goal-directed," or likely to b e
amenable to neurophysiological analysis, but because some
animals and behaviors allowed relatively efficient collection of
data appropriate to the particular scientific questions the ethologists were asking. These questions appear to have revolved
largely around the role of behavior in evolution. Thus "speciesspecific" behaviors, such as mating rituals (which lent themselves to analysis of behavioral homologies), were of lnorc
evolutionary interest than behaviors, such as flexion reflexes,
locomotion, or scratching, that appear identical across many
species. Stereotyped, all-or-none behaviors were useful because they simplified quantification and optimized observability. The species selected were almost always easily accessible for naturalistic observation. As bird watchers, butterfly
collectors, and naturalists well know, colorful, diurnal, flying
animals with dramatic behavioral displays (i.e., many birds and
insects) are easy for people to observe in the wild. That does not
mean that these same species and behaviors are also optimal for
neuroethology, nor does it mean that ethology should restrict
itself to the convenient classical preparations. As modern ethologists have extended their studies to less theatric behaviors
and animals, they have found that restrictive definitions of
ethological terms such as fixed action pattern, releaser, and
consummatory act have limited applicability in many situations
(Hinde 1970). Moreover, these definitions are really of less
importance than the larger goals of ethology, which are to
understand the biological adaptiveness of behavior and its role
in evolution (Lorenz 1958).
Hoyle seems to have overlooked the zoological and evolutionary heart of ethology in his prescription for neuroethology.
Instead, he offers a set of goals that fits better into other areas of
neurobiology: motor control and pattern generation, sensory
and perceptual physiology, learning and memory. These areas
of neuroscience are defined by functional questions, not by a
priori definitions of innate fixed action patterns or by simple
reference to the supposed tastes of the field's pioneers. If there
is to be a science of neuroethology distinct from the rest of
neurobiology, it must first identify the central goals (rather than
the methods and prejudices) of ethology that will benefit from
neuronal analysis. I submit that these goals should not be
directly concerned with the physiological mechanisms ofbehavior (which are the province of neurophysiologists and neuropsychologists), but instead with the complex interactions among
evolution, the nervous system, and behavior. Such goals might
concern the processes by which the nervous system provides
adaptation to an animal's niche; the neural substrates by which
phylogeny, ontogeny, and learning interact to produceadaptive
behavior; and the sites of neural change underlying changes in
behavior during speciation. Having set general goals, the neurocthologist then selects the preparations that promise "easy
accessibility" to the specific questions asked in order to move
toward each goal. Preparations that are practical for the combined analysis of genetic, developmental, and cell biological
correlates of behavior should be especially useful for neuroethology, and I agree with Hoyle that insects are attractive for
certain neuroethological questions.
However, different neuroethological qucstions will lend
themselves to different preparations, and it seems premature to
discard most of the animal kingdom in favor of anybody's
"optimal" neurocthological preparation. Despite Hoyle's suggestion that "no principles of integrative or intrinsic neural
functioning" have come from Aplysia (which seems strange in
view of his other statement, "Much of our knowledge of basic
cellular neuronal properties has been derived from Aplysia"), a
variety of general principles of neural function related to the
scope of neuroethology have come from Aplysin and other
gastropods. My pet example is activity-dependent neuromodulation, which was first discovered in Aplysin in its tail
sensory neurons (Walters & Byrne 1983) and shortly afterward
in the siphon sensory neurons (Hawkins, Abrams, Carew &
Kandel 1983). This mechanism allows the selective addressinp
ResponselHoyle: Neuroethology
of hormones or neurotransmitters to functionally active cells,
small cells in a truly "higher invertebrate," which I could easily
providing a mechanis~nfor associative learning and offering the
Surely we study simple systems for two reasons: (1) because
possibility that similar addressing of trophic signals occurs
they are important in themselves, for example, in insects,
during development. Activity-dependent neuromodulation
may be quite general, having also been found in the crayfish
andlor (2) because they help us to understand the nervous
(Breen & Atwood 1983); suggestions of it have been reported in
system and behaviour. For this latter purpose, neuroethology
has presented us with some fine analytical tools, especially fixed
the mammalian brain as well (Woody, Swartz & Cruen 1978).
action patterns and releasers. But its more general theoretical
Although (as I have defined neuroethology) few neuroethological questions have been addressed directly in thc
models, such as action specific energy, seem to me to obscure
easily accessible gastropod nervous system, the gastropods
the problem and hinder proper analysis. Hoyle's criticism of
"relfex physiology" and the rest seems old-fashioned when
seem well suited to a neural examination of at least one of the
ethological questions that most occupied Lorenz, that of the
experimenters like Mountcastle and Zeki, theoreticians like
Marr, surgeons like Ojemann, and psycholdgists like
relationship between innate and learned adaptation to the
environment, sometimes viewed as the "nature-nurture" conWeiskrantz and Milner are greatly advancing our knowledge of
the difficult problems of the nervous system. Unfortunately,
troversy (Lorenz 1965). The fact that gastropods show fixed
most zoologists pay no attention to such people. They would do
action patterns that can b e regulated by associative learning
(e.g., Walters, Carew & Kandel 1981), as well as su~yrisingly better to heed them and stop criticising poor old Sherrington
complex forms of classical conditioning (Sahley, Rudy & and Pavlov, who did well enough in their day. I fear that
emphasis on "neuroethology" will further isolate zoologists,
Gelperin 1981), and memories that can last for weeks or months
(Croll & Chase 1977; Pinsker, Hening, Carew & Kandel 1973)
which would b e a pity.
Hoyle himself has done splendid work on memory, which
augurs well for the possibility of obtaining insights on the
seems to me to contradict the whole tenor of his target article
cellular level into the processes by which learning interacts with.
instinct. In addition, the gastropods provide easy accessibility
for the zoological, developmental, and genetic investigations
(Kandel 1979; Kriegstein 1977; McAllister, Scheller, Kandel &
Axel 1983) that will be necessary for securing answers to this and
other general neuroetl~ologicalquestions.
Author's Response
Is neuroethology wise?
J. 2. Young
Neuroethology: To be, or not to be?
The Wellcome Institute for the History of Medicine, London NW1 ZBP,
Graham Hoyle
I cannot help continuing to feel out of sympathy with the
attempt to construct a distinct science ofneuroethology. I agree
with the need to correlate studies ofnatural behaviour with their
netlral backgrounds. It is clearly valuable to recognise subroutines such as fixed action patterns (FAPs). But what is gained
by making a special science of this study and isolating it from
other studies of behaviour? In particular, it seems most unwise
to concentrate so much on the inherited component of behaviour. Hoyle himself seems confused about this. His definition ofprimary targets for neuroethology deals with "instinctive
acts." But by the second paragraph of "Is a general theory of
neural circuit function possible," "memory" is the first of his
possible neuroscience clusters. Presumably, this is not to be
part of neuroethology, since memory is not instinctive.
Another danger in isolating the study of FAPs is that it
obscures the need for the study of coding. Hoyle rightly castigates those who limit themselves to small parts of the nervous
system and regrets the lack ofageneral framework to replace the
"McCulloch-Pitts (1943) binomial model." Surely this lack is
due to overattention to simple systems in which the coding
problem seems soluble. He rightly says that we need attention
to the dgicult problems ofco~nplexsystems. Yet the program of
neuroethology concentrates on simple problems almost by definition. He puts "in-depth analyses of the neural machinery
producing FAPs" as his first priority.
A further worry about neuroethology is that it has encouraged
people to work only with animals that have large cells that allow
intracellular recording. The really deep problen~sare in the
systems with small cells; if they cannot be analysed by way of
electrodes, we must find other methods. In fact, each animal
and group of workers contributes differently. Hoyle ridicules
Aplysia as a "glob of squishy protoplasm," but, with it, Kandel
(1976) has taught us the only hard facts we know abont memory,
because of one small cell in it. Now we need the study of many
Institute of Neuroscience, University of Oregon, Eugene Oreg. 97403
First, I should like to thank all of t h e c o m ~ n e n t a t o r sf o r
taking t h e t i m e t o read m y article a n d t o prepare such a n
interesting array of commentaries, n o t forgetting t h e
several persons whose commentaries w e r e received l a t e
and a r e not included h e r e f o r lack of t i m e and space.
Perhaps I shall h a v e t h e opportunity t o reply t o you i n
Continuing C o m m e n t a r y . I feel greatly honored by t h e
interest of s o m a n y distinguished scholars in m y (as
several of you wrote) " idiosyncratic musings." My only
comfort in t h e face of this p r e s u m e d criticism is t h a t t h i s
expression would apparently have b e e n equally applicable t o others a m o n g you, h a d you b e e n t h e author. I a m
grateful that t h e titles o f only two of t h e commentaries
included t h e inevitable reference t o t h e best-known
bearer of t h e family n a m e !
I t d o e s n o t surprise m e that very few of y o u a r e
empathic with m y specific proposals. S o m e of you, like
o n e of m y ex-Ph.D. students, Macmillan, a major m e n tor, Young, a n d Erber, d e t e c t "contradictoriness, inconsistency and dissonance." Perhaps this apparent fickleness is inevitable w h e n o n e is groping for articles of faith: I
would truly like t o be a disciple of a c o h e r e n t discipline of
neuroethology. T h e commentaries m a d e it clear t h a t it is
a t best going t o be m u c h m o r e difficult than I had t h o u g h t
for u s to achieve a consensus a s to the kinds o f studies t o
b e incorporated u n d e r t h e r u b r i c neuroethology. C l a r a c
addressed t h e intrinsic difficulties of makine:
" neuroethological studies n o m a t t e r h o w w e define them,
while Young believes it u n w i s e e v e n to consider t h e use o f
this designation as a subdivision of neuroscience.
The most commonly expressed objection to my proposals was a desire to remain free to adopt any connotation now, or at any time in the future. Bullock aptly
expressed this view with his "don't fence me in" title.
However, neither Bullock's arguments nor those of the
others expressing this viewpoint, notably Bassler, Davis,
Ewert, Steklis, Simmons, and even Huber (who, like
myself, works on insects and is also now pushing for
identified neuron work) have persuaded me away from
my premise, that restriction is necessary. I willingly
concede that my own definitions and list of goals are open
to criticism. If there were a consensus as to what we
should do in the name of neuroethology I should be glad
to conform and either follow or alternatively adopt the
label of whatever branch of neurobiology you assign to
me. Bassler suggests Sensomotorik, but while this expression is true of what most of us do in practice, the
missing element is clearly the dedication to behavior. I
want a close relation to the search for, and the understanding of, general principles (always assuming there
indeed are any) underlying the neural generation of
behaviors. It is apparent that you all share my unease with
the situation in which we currently find ourselves, in
identifying the subject matter of neuroethology, whatever your individual bias, in both research and in teaching. Some of you are content to let matters drift for the
time being, as though they will sort themselves out quite
naturally, with time. Of course, I strongly dislike this
viewpoint, as my target article emphasized, perhaps
because time is running out.
To Young I assert that since the term neuroethology is
now the title of four books, albeit each with very different
contents, it is unlikely to fade away. Incidentally, the
newest to arrive on the scene (Camhi 1984) provides
another difficult pill to swallow. Expressly avoiding the
desperately needed "broad, comprehensive treatment
covering a great many of the animals that have been
studied" (from the Preface), Camhi provides us with a
largely elementary introduction to neurobiology as a
whole, rather than a well-defined subdivision. The intrinsic paradoxes of attempting to define neuroethology and
to prepare experimental protocols arising out of the
definition were addressed by several of you, perhaps
most eloquently by Bateson, Although I took a strong
stance, which was at least in part based upon personal
conviction, admittedly biased, and of the die-hard variety, I hoped to provoke you into suggesting alternatives,
one or another of which might become widely accepted.
This was my principal disappointment with the commentaries. Although most of you grumbled about my specific
proposals, none of you presented comprehensive
Erber objects to my lack of details on the hypothetical
"comparator" and "computer" elements of the updated
hydraulic model I proposed in Figure 4 of the target
article, for which several of you expressed dislike. Of
course, nobody knows what the elements might be, but
the terms have been used quite frequently in recent years
by neural theorists, so there seemed no need to explain
them. My intention was to draw attention to the urgency
for experimental neuroethologists to be aware of the need
to provide some substantive locales for these processes in
the simpler invertebrates which possess them. Ifany sets
of neurons serving these functions can be found, studying
how they work would become a major research target for
neuroethologists. Erber refers to the new hydraulic
model of Lorenz (1981), which is reproduced here in
Figure 1. Lorenz chastises himself in his new book; The
Foundations ojEthology, for not having realized that his
early model (Figure 3 of the target article) had what he
chooses to call a major deficiency - the model misleadingly implied a qualitative difference between events
that fill the tank with "energy," and those that release the
behavior, when they in fact "differ only in quantity." I
found this "confession" and "correction" quite sad, because the old model closely depicts the situation for some
behaviors with which I have worked whereas the new one
does not. The new Lorenz model is a throwback to the
dark ages of total reflexology! Ifwe have found anything at
all that is truly worthwhile in the name of neuroethology
it is that there are manv behaviors for which the readiness
to execute a particular behavior is determined by endogenous mechanisms that are totally independent of particuJar kinds of sensory input or even, perhaps, any input at
Lorenz reiterates that "some sort of motor excitability
accumulates while a motor pattern is not performed and
then used up by its performance" (p. 286). He also states
emphatically that "the concept of a specific quantity of
excitability obviously corresponds to a physiological reality" (Lorenz 1981, p. 122). With both of these statements
I agree, except that, as Lorenz himself points out elsewhere in his book, the first would have been more
inclusive had it read: "some sort of motor excitability
accumulates in some behaviors when motor patterns are
not performed and then used up by their performance."
Lorenz avoided stating what h e thought might be the
neural substrate of action-specific energy (which he now
prefers to call action specific potential, ASP), although
hinting at the involvement of neuroactive substance(s).
Figure 1. Lorenz's (1981) revised version of his classic
hydraulic model (see Figure 3 of the target article). Asp represents Action Specific Energy, ER an endogenous readiness
agent, AR accessory readiness agents, and SR the releasing
stimulus. In the earlier model SR was depicted as weights added
to a scale pan attached via a pulley wheel to the stop at the base
of the tank. From Lorenz (1981);reprinted by permission of the
The gradual accumulation of ASP from the constant
dripping of the endogenous source is readily associated
with a gradual build-up of a neuromodulator in appropriate neurons, as outlined in my own orchestration hypothesis. When a behavior is released, the appropriate cluster
of modulator neurons is excited. Their stores of modulator substance are depleted as the behavior, which they
help to generate, unfolds.
The emergence of the new model from Lorenz further
emphasizes my key point, which is that the core of
neuroethology should be to examine the model in relation
to a variety of behaviors, from diverse phyla, in depth, by
way of cellular neurophysiological analysis.
In his new account, Lorenz has made another shift in
msition which I consider to be a serious error from the
ioint of view of neuroethology. He has chosen to substitute the expression fixed motor pattern (FMP) for fixed
action pattern (FAP). This is most unfortunate, because
the former expression begs an important question. In the
parlance of (Hoylean) neuroethology, a FMP means that
the CNS produces a motor output that is tightly controlled in regard to the numbers and timing of motor
impulses. Highly stereotypic outputs are known, for
example, in cricket songs, as demonstrated first by Ewing
and Hoyle (1965), and then very beautifully developed
using genetic procedures by Bentley and Hoy (1974). An
even more remarkable example of stereotypy occurs
during courtship behavior of the tiny male grasshopper
Gomphocerippus rufus and its relatives, reviewed by
Elsner and Popov (1978). These studies have shown that a
nervous system can produce stereotyped motor output
accurate to the level of a single nerve impluse, with 2 1
millisecond accuracy in timing. Such sequences are true
FMPs; some are produced in the absence of any external
stimulus, others only when a specific single releaser (sight
of female) is present.
Fixed action pattern (FAP) is the appropriate general
term because, for a majority of stereotyped movements,
even in insects, the underlying motor patterns (which is
to say, the electrical activity in the motor neurons causing
the movements) are not fixed even though the movements (actions) are. In 1954-55, I recorded the electromyograms of several thousand visually identical, stepping movements from locusts induced to march under
laboratory conditions (Hoyle 1957). Off and on since then
I have repeated this work and have recorded from walking insects of other species also. The almost incredible
fact is that no two out of the thousands of EMGs recorded
- these indicate the motor patterns causing limb movements, which even high-speed cinematography shows to
be identical in mace and time - have exactlv similar
underlying motor patterns. There are periods when only
intrinsic muscle tonus, a very significant but totally neglected factor, together with inertial and gravitational
forces, are the only antagonist to phasic agonistic action
(Hoyle, 1984). At other times there is constant-frequency
antagonist excitation, requiring much more powerful
agonist excitation to achieve the same movement (Figure
2). At yet other times, perfect reciprocity. of antagonists,
with no overlap, occurs, or there can be extensive
The point is that the movements can be "fixed" even
though the motor output is anything but fixed. These
experiences led me to propose (Hoyle 1964) that in many
I '
Figure.2. Electromyographic activity in the antagonist muscles causing alternating flexion and extension ofa locust hindleg
extensor tibia, during a bout of rhythmic stepping at a mean
frequency of 1.2 per second. The flexion movements wcrc
caused by bursts of impulses in a complex of three intermediate
flexor and three fast flexor motor neurons. The individual
contributions of these neurons were different for each flexion.
Extension was produced during each waning of flexor activity,
because the slow extensor motor neuron SETi fired throughorlt
at a nearly constant frequency averaging 19 Hz. Thirty stepping
movements are included in the record shown (top traces excerpt at higher speed below), each of which was visually
identical. From Sombati and Hoyle, unpublished.
FAPs the motor program must be guided by a CNS store
of sensory information. This I termed a "sensory tape"
mode of operation, the information content being equivalent to a score, consistingof the appropriate sequences of
sensory inputs associated with the movements to be
programmed. The store of information is conceptually
equivalent to musical notation. Neuroscientists often
think of musical notes as motor instructions, which they
are not. They are no more than sensory guidelines,
indicating what has to be achieved by an independent
comparator with computer feedback and a motor output
In presenting his new hydraulic model Lorenz presciently foresaw my own version of his model when he
wrote, "The simulation could be brought closer to the
real physiological process by adding a few gadgets." In my
model, replete with gadgets, and in the text, I also placed
a high priority on understanding the locations and natures
ofstored information, whether inherited or acquired, and
how such data are addressed and fed into the nervous
system as needed. This has been attacked by Bateson as
being both naive and irrelevant. It is indeed possible that
there is no separate section of a nervous system which is,
as it were, set aside specifically to take care of these
functions, and that they are distributed among the entire
neuron population. Yet Young approached the Octopus
nervous system as though it were compartmentalized and
found that this was indeed the case. We need comparable
studies on other organisms. If equivalent data were available for an invertebrate with complex behavior, yet a
nervous system well described at the identified neuron
level, then I believe we could, for the first time, get an indepth grasp of how nervous systems produce complex
Fernald and Ingle both accuse me of being unaware of
the elegant work of fellow Oregonian Bell, on "efference
ResponselHoyle: Neuroethology
copy" in weakly electric fish (Bell 1981). I am sure,
however, ,that Bell would be the first to come to my
rescue, since he knows that I admire his work, and
likewise that of Bullock's associates on these fish. Bell
provided incontrovertible but indirect evidence in a
vertebrate for the existence of an efference copy of motor
output (to the weak electric organ). Many years earlier I
showed that a locust ganglion must keep an efference
copy ofany significant trends that occur in mean frequency of its tonic motor output (Hoyle 1965). If such shifts in
frequency are consistently correlated with aversive inputs, then an adaptive process is set in motion, which
reverses the trends. One of my pleas in the current target
article was for work to be attempted on the physical
location and cellular nature of efference copies, a matter
which Bell has not addressed, and about which nothing is
known. Knowing the physiology of efference cogies is
profoundly important for understanding the neural details of behavior generation.
To Rowell I should like to say that I was a close personal
friend of Wiersma from 1955 until his death; I worked
with him at Caltech in 1956-57, and as Rowel1 knows,
since he was there, I organized a Wiersma festschrift,
which was published in 1977. I am certain that Wiersma
enjoyed as great an intellectual intimacy and empathy
with me as with any other scientist. He greatly influenced
my thinking, but there was also a lot of intellectual traffic
in the other direction. I am the last person in the world
who would willfully denigrate Wiersma's pioneering
efforts. However, I am certain that at no time did he ever
think along the same lines I have, or published concerning the neural bases of behavior. Incidentally, he was as
dismayed as I have been at the frequent misuse of his
concept of "command" interneurons. [See Kupfermann
& Weiss: "The Command Neuron Concept" BBS l(1)
Ewert accuses me of missing out on comparative aspects, but I should like to remind him that I have
published neuroethologicaI data on sixteen species, from
six different phyla. However, while I greatly enjoy the
diversity, it has given me less than 1 had hoped for in the
way ofworthwhile insights into what I really want to know
about how nervous systems work, because so much is
always unknown. It will be essential for many investigators to stick with related aspects of one species for a very
long time if the requisite depth of information is to be
attained. Of course, that which is indeed general must be
extracted after making comparisons, as I have often emphasized. A major "message" of my target article is that
many of those collecting data in the name of neuroethology are not yet even trying to collect the most
needed data, because they do not adequately focus their
efforts on core problems. The vertebrate neuroethologists among you acknowledge that they are concentrating on sensory aspects because of technical difficulties in bridging the all-important gap to the CNS
integrating regions, with their memory stores, comparators, and computers.
In a positive vein, may I say that I appreciated the
wisdom offered by Steklis, Walters, and my colleague,
Simmons. You have tempered my steel! I am more than
grateful to Manning, Grossberg, Huber and especially
Markl for the much needed kind remarks interspersed
among their legitimate criticisms. Even in Science an
ounce of praise sometimes produces more useful activity
than a ton of kicks!
In reply to Guthrie's inquiry regarding the orchestration hypothesis, we are working intensively on this, and
its consequences, in the locust, and we have had some
very exciting results, but we are a long way from being
able to present a complete picture for any single behavior. One of the orchestrated behaviors we are studying is
flight (see commentary of Rowell). In the locust, to our
knowledge, there are only two substances which mediate
the orchestration of metathoracic ganglion behaviors:
octopamine and proctolin. There are about 90 octopaminergic neurons and only a few that are proctolinergic, so octopamine is by far the more important.
Vertebrates have a whole pharmacopoeia of modulators. I
do not consider that a modulator substance corresponds
to a section of a "tape." Each modulator is discretely
released at from one to several highly localized sites, in a
precisely timed sequence, by from one to several modulator neurons. These events in totality represent the tape
playback. A single synchronous burst of excitation of a
subcluster of modulator neurons, whether using the same
or different substances, elicits the equivalent of a single
tape section. Where the store of information is located
that ~ e r m i t scontrol of the activity of the modulator
neurons seems likely to become a key question for
What may 1 say in attempting to annul the bad taste I
consciously courted by my acrid remarks concerning the
future of vertebrate neuroethology? Ehret tells me, simply and clearly, how I could have modified the target
article so as to make it widely acceptable, which of course
I should have liked, but drily up to apoint. The worldwide
ratio of neuroscientists working on vertebrates to those
working on invertebrates is greater than 30:l. The size of
the splash made by invertebrate neuroscientists in the
last decade is out ofall proportion to the share of the total
funds made over to them, and is a real tribute to both the
accessibility of identifiable neurons in some invertebrates
and the strategies adopted for exploiting them. Young,
and indeed some other commentators. too. associate
neuroethology largely or exclusively with in"ertebrates
because of this. I'm sorry that after devoting a lifetime of
unparalleled, superb work on cephalopod brains, which
are the most advanced physically among invertebrates,
Young's efforts are not being rewarded in the form ofany
cellular-level progress made with them.
The principal reason for adopting the position I did
regarding vertebrate studies is that the more one knows
about what it is that has to be known before one can
satisfactorily describe how a behavior is generated and
controlled, the more the focus becomes cellular. Diagrams such as that of Weiss (1950) (Figure 2 of the target
article), which was adopted by Baerends (1976) and included by Lorenz in his new book, may be conceptually
expressive. But they are meaningless in terms of neural
anatomy and physiology while implying the contrary. In
the long run there can be no substitute for knowledge of
the properties of individual neurons, their connections
and interactions and modulations thereof, which are
active in behavior. None of these can b e second-guessed,
but must be determined directly. Furthermore, while we
may find it useful to build tentative models on the basis of
early findings even in systems with few neurons, we must
ResponselHoyle: Neuroethology
insist that no neuronal "stone" remain unturned. In the
latest appraisal of functioning of the 30-neuron lobster
stomatogastric ganglion, no fewer than 5 different modulators, dopamine, NA, 5-HT, and two peptides, have
become implicated (Eisen & Marder, in preparation). All
early models are currently being overthrown in light of
findings about the actions of neuromodulators. Someday,
a better understanding of the contributions of intracellular rather than extracellular information transfer is
likely to have even more profound effects on our thinking.
Ingle, and others of you who work on vertebrates
cannot expect any sympathy from me! There may be a
case for associating neuroethology specifically with invertebrates, but for the converse exclusivity, as expounded
in the recently published book, Advances in Vertebrate
Neuroethology (Ewert, Capranica & Ingle 1983), I can
find no justification. There are marked differences in
neuronal organization, of course, between vertebrates as
a whole and any single invertebrate phylum. The almost
universal tendency to lump invertebrates together is
biologically absurd. There are greater differences between molluscs and arthropods than there are between
arthropods and vertebrates, because molluscs lack a skeleton and jointed legs. The range of neural organizations
seen within a single phylum, especially the molluscs,
which is the most diverse of all, is vast. But in the matter
of the principles of behavior generation, which I maintain
is the major objective of neuroethology, who among you
expects major differences to be found? Once again I
reiterate that we should focus on possible common
Our endeavor, almost unique in biology today, has the
opportunity to benefit from a genuinely comparative
approach, which I do indeed favor strongly. This should
not be seen as yet another dissonance on my part. Indepth studies on vertebrate neurobiology are going to
continue no matter what. It is support for the invertebrate studies that needs understanding and sympathy
because it will always be fragile and vulnerable and can so
easily suffer from neglect in the future. Even if studies on
invertebrates do continue to prosper, unless there is
intellectual reciprocity, both between those who study
them, interphyletically, within invertebrates, and between each of these persons and the majority, who are
studying vertebrates, we shall never have a true science
of neuroethology.
Curiously, some of the greatest discord is to be seen
among those who work exclusively on a single invertebrate species. Each waves the flag of chauvinism, espousing some "unique advantage," but actually trying to draw
attention to his or her own work. To a large extent it
relates to the demeaning practice of being required to
'j'ustiFy" the expenditure of money on basic research.
A major secondary consideration in this regard is
laziness. It is easiest to avoid burdening our overloaded
brains with the work of others, concentrating instead on
"getting results" and "getting them published." When
the work of others directly relates to our own because it is
on the same part of the same species, we must pay
attention. But otherwise? We are producers, but where
are the consumers? The only possible consumers are
ourselves; we should all consume a lot more than we do
currently if we are to survive.
Of longest acquaintance, and a most trusted friend is
Manning, who pointed out that perhaps you need to
understand the sociology of the dominant Viking element
in northern England in order to appreciate a target article
written bv one of them! Yet at the north-countrv grammar
school which most shaped my character, almo>;'the first
lesson was that we should follow Socratic principles:
Dialectic was said to be the essential basis for anv intellectual endeavor! When my first debate teacher, a very tall
Scotsman named Murdoch, with bright blue eyes and a
shock of red hair. first addressed me. he said: "Youne"
Hoyle, you're enthusiastic about the time-honored sport
of fox hunting, are you not?." "Oh no, sir,'' I pleaded
passionately, "I believe it to be cruel, beastly, socially
irresponsible, and in every way obnoxious!" "Splendid,"
he retorted, "for next week's debate you will be the
proposer of the motion that this house strongly favors the
perpetuation of fox hunting. Trying desperately hard, at
a tender age, to understand the other person's point of
view and defending it in public debate with a professional
advocate's urgent desire to win as a matter of principle
(we lost) was an invaluable lesson for life. No wonder I am
an ardent supporter of BBS.
So I esaeciallv thank those of vou from whom I learned
a new viewpoiit: Arbib, ~ a t e s b n and
Grossberg. You
are absolutely right about our exclusivity and lack of
cross-fertilization. I have started to immerse mvself in
your lists of references, insofar as these are available to
me. You may be surprised at how few are to be found in
the library of the university where I work, a major, statesupported university no less. -This is an important point:
The serious theoretical work in neuroscience, which I
strongly advocate in my target article, must be published
in coinmonly aoailable journals of neuroscience, not hidden in "U. Mass. Technical Reports," "Air Force Ofice of
Scientific Research Reports," and obscure books which
impoverished university libraries cannot afford to
We certainly need to get together more, and often. A
splendid beginning was made more than two decades ago
in the symposium, which I was fortunate enough to
attend, held at Ojai, California, in 1962, which led to the
book edited by the late Reiss entitled Neural Theory and
Modelling. Some of the papers published in this pioneering blend of theoretical and experimental approaches are
still referred to quite often today. But where are the
sequels that might have kept this early interdisciplinary
endeavor up-to-date? Theorizing is not an aspect which
has stood still; it is contact with the rapidly advancing
knowledge of nerve cells and circuits - especially motor
circuits - which has lagged. At this point I should like to
defend my not paying much attention to the work of von
Holst. In part this was because of the direction his work
has taken, as exemplified by his student, colleague and
successor at Seewiesen, Mittelstaedt, who has, with others, made theorizing about neural function in behavior an
end in itself. This activity is doomed to sterility unless it
can be linked to identified neurons. I t has fostered a
specific subdiscipline boasting two journals, Kybernetik
and Biological Cybernetics. I shudder when I think back
on the time I have spent struggling through the often
mathematically difficult papers in these journals in search
of illusive enlightenment.
One can but marvel at the versatility of Poggio and his
associations with the late, prophetic David Marr, on the
ResponselHoyle: Neuroethology
one hand, and Reichardt, on the other. The latest paper
by these authors (Reichardt, Poggio, & Hansen 1983) is
tantalizingly subtitled "towards the neural circuitry" (of
the flight control ofa fly by visual input). May I live to see
the day when these worthy theoreticians guide a capillary
electrode into a neuron! Thev will certainlv be welcome
additions to the inner core of neuroethologists.
Similar thoughts go out to Hampson and Kibler (1983)
in their efforts to establish a Boolean neural model of
adaptive behavior; likewise to Pellionisz and Llinas
(1979), Morasso (1981), and now even the psychologist
Fentress (1981), in their very different approaches to the
question of recognizing that behavior is a three-dimensional movement domain. It would be of no value to
imply, given the minuscule amount we currently know
about nervous systems, that strictly artificial intelligence
research is outside the range of neuroethology. Few of us
have failed to be impressed or even influenced by Minsky
and Papert's (1969)classic book on perceptrons, or Klopfs
recent The Hedonistic Neuron (Klopf 1982), which
shows that at least some theoreticians know and relate to
some cellular neuroscience.
Some of you, notably Hinde, Manning, Schleidt, and
Fernald, protest that I have not kept up with the progress
in ethology. This is doubtless true, and perhaps I misread
the various articles recommended to me by way of catching up, including those in the series Perspectiues in
Ethology edited by Bateson and Klopfer. Or it may be
that I was unable to tear my mind away from early
ethological imprintings. It seemed to me that recommended articles were ~rovidinrrevasions. circumlocutions, apologies, and reinterpretations of the most diffuse
kind. They did not replace old concepts with new ones:
The basics clearly remain the same. If there are no hardcore general principles underlying behaviors, then the
party is over: There can indeed by no neuroethology, at
least not a worthwhile intellectual endeavor demanding
serious effort. However. I was not convinced of this bv
what I read. I believe that the program for neuroetholoh
which I propose in my target article has the merit that at
least it would help to settle the question ofwhether or not
there are common ~ r i n c i ~ l of
e sbehavior. which cannot
be resolved by stridtly behavioral researdh. Disciplined
neuroethology would be of inestimable help to ethologists in the long run. Because of the constraints dictated by neural functions it would clarify the nature ofthe
different kinds of behaviors studied by ethologists, and
promote rational classification.
To the highly perceptive Markl, and also to Delcomyn
and Bateson, go my special commendations for, as it
were, seeing through me. The article was indeed a kind of
sermon. This field needs a new kind of funding: assured
basic funding for long periods, preferably measured in
terms of a human working lifetime.
To those of you who have worked intensively on a
ganglion selected entirely for its manipulative convenience, specifically Kspfermann, Leonard & Lukowiak
for the Aplysia visceral ganglion, and Selverston for the
stomatogastric of spiny lobsters, may I say only "please
render unto Caesar . . ." I greatly admire your beautiful
work, which I always read carefully, and I do listen to
your sessions at meetings ofthe Society for Neuroscience,
as you surely know. What is available in the catalogue of
cellular and synaptic mechanisms and modes of hooking
up of neurons is potentially core material for neu<,
roethology. However, I note that these sessions tend to
be dedicated to "transmitters," "synaptic transmission,"
and "circuitry." Also, you show a preference for the
Journal of Neurophysiology as a publication outlet. As I
see it, your goals seem to have been primarily toward
ex~osinecellular events as ends in themselves: Where is
t h l dedycation to understanding the broad principles of
behavior? Where are the comparisons and discussion of'
the relevance of your findings to those of others working
on different phyla? Admittedly, there is a seductive
cellular trap (and a comfortable one, because considered
significant), that I also fall into, as I pointed out in the
target article. When I was preaching in the target article,
it was as much at myself as at any of you.
The plea is for us to recognize the possibility of a
subdivision of inauirv that is more than something.,
thrown in as an afterthought, as so often appears to be tke
case with our existing neuroethology. The objectives of
neuroetholoeical research should be clearlv stated and
relentlessly pursued, in animals selected for their relevance, not the convenience of some small part of their
nervous system. The "behavior" of Aplysia has been
concocted by neurophysiologists, not, as Leonard &
Lukowiak point out, by ethologists. The latter are not
about to switch to studying Aplysia, and elevation of the
movements performed by this mollusc to the presumed
status of serious ethological interest, if done solely by the
neurophysiologists themselves, is not likely to cut any
My final specific reply is reserved for ethologist
Bateson. Yes, I am truly willing to let ethologists be the
pipers and call the tunes. But in exchange, they must read
the work of neuroethologists closely, understand the
capabilities and limitations neurophysiologists face technically, and be willing to focus their own attention on
behaviors of neurophysiologically tractable animals.
I am ready to take seriously any model which treats
generation of
nervous svstems as devices for the intrinsic "
behavior as their primary purpose. Inputs which promote
general or specific behaviors, o r which modify ongoing
behavior, or which are anticipated and incorporated into
the generation of specific behaviors, are superimposed
upon an intrinsic capability. We must reject all models
(they are the majority) that treat nervous systems as if
they were inputloutput devices.
Amari. S. & Arhib, M. A,. eds. (1982) Conlpetitio~land cooperation in ncbtrral
nets. Lecture Notes in Biomathei~~atics
45. Springer-Verlag. [MAAI
Arbib, M. A. (1972) The ~mtaphorica/6roirr: AJIintrorltrctio~~
to cybernetics ns
artifcia! intelligence and brain theonj. Wiley I~~terscience.[MAA]
(1981) Perceptual structures and disturl)cd motor n~ntrol.In: IIa~tdbookof
physiology, Section on neurophysiology. Vol. 2: Motor cotttrol, ed. V. B.
Brooks. American Physiolopical Society. [MAAI
Angel, R. W. (1976) Effercnce copy in the control of tnovemet~ts.Nctrrokrgy
26:lIM-68. [HDF]
Baerel~ds.G. P. (1976) The h~nctionalorganization of hchavior. Ar~irr~al
Behatiwur 24726-38. [RDF, rCHl
Ballard, D. & Brown, C. M. (1982) Cwnyrrter ci.sio~t.Prenticc-Hall. [MAAI
Barlow. G . W. (1977) Motlal action patterns. In: Ilot~.anirnab cointntrrticnte.
ed. T. A. Seheok. University of Indiilna Prcss. (taCHI
Barlow, H. B. & Levick, W. H. ( 1 9 6 ) The m~rhanis~n
of directio~~ally
selective nits in rabhit's retir~a./otrrrral of Pl~~/.~iolo.g~,
London 178:477FjW. ICHFR]
Bnrnett, S. A. (1981) Morlrr~rethulo.g!/: TIze .rcirrlce r,fn~~imn/
Oxford University Prcss. [taGH]
ReferenceslHoyle: Neuroethology
Bgssler, U. (1983) Neural basis of eleinentay behacior in stick insects.
Springer-Verlag. [UB]
Bastock, M., Morris, D. & Moynihan, M. (1953) Some comments on conflict
and thwarting in animals. Behaciour 6:66-84. [RAH]
Bateson. P. (1983) Genes. environmcnt and the development of behaviour.
In: Animal behaciour. vol. 3:Cenes, development and learning, ed. T. R.
Halliday & P. J. B. Slater. Blackwell. [PB]
Bayliss. L. E. (1960) Principles of general physiology. Longmans. Green &
Co. [DMG]
Baylor, D. A. & Hodgkin, A. L. (1973) Detection and resolution of visual
stimuli by turtle photorecwptors. lournal of Physiology 23416398. [SG]
(1974) Changes in time scale sensitivity in turtle photoreceptors. journal of
Physiology 242:729-58. [SG]
Baylor, D. A., Hodgkin, A. L. & Lamb, T. D. (1974a) The electrical
responses of turtle cones to flashes and steps of light. lournal of
Physiology 242:685-727. [SG]
(1974b) Reconstruction of the electrical responses of turtle cones to flashes
and steps of light. lournal of Physiology 242759-91. [SG]
Bell, C. C. (1981) An efference copy which is modified by reafferent input.
Science 214:450-53. [RDF, rCH]
(1982) Properties of modifiable effercnt cells in an electric fish.]ournal of
Neurophyswlogy 47:1043-56. [DJI]
Bent, S. A. & Chapple, W. D. (1977) Simplification of swimmeret musculature and innervation in hermit crab. Pagurus pollicarpus, in comparison to
Macrurans. Journal of Comparatiw Physiology 118:61-73. [FC]
Bentley, D. R. (1971) Genetic control of an insect neuronal network. Science
174:1139-41. [taGH]
Bentley, D. R. & Hoy. R. R. (1972) Genetic control of the neuronal network
generating cricket song patterns. Aniiiurl Behaciotrr 20:47&92. [taCH.
(1974) The neurobiology of cricket song. Scientif~ American 231:3442. [&HI
Black, H. S. (1934) Stabilized feedback amplifiers. Bell Systerns Technical
Journal 13:l-18. [DMG]
Block, C. H . , Siegel, A. & Edinger, H. (1980) Effects of amygdaloid
stimulation upon trigeminal sensory fields of the lip that are established
during hypothalamically elicited quiet biting attack in the cat. Brain
Research 197:39-55. [HDS]
Boeckh, J.. & Ernst, K. D. (1983) Olfactory food and mate recognition. In:
Neuroethology and behacioral physiology, ed. F. Huber & H. Markl.
Springer-Verlag. [JE]
Breen, C. A. & Atwood, H. L. (1983) Octapamine - A neurohormnne with
presynaptic activitydependent effects at crayfish neuromuscular
junctions. Nature 303:716-18. [ETW]
Brown. Boveri & Cie. (1982-1983)The OMS-vision system. Technical
information sheets DNG334380E and =ID.
Brown, J. L. & Hunsperger, R. W. (1963) Neuroethology and the motivation
of agonistic behaviour. Aniinol Behaciour 11(4):439-48. [HDS]
Bullock, T. H. (1977) Introduction to nen2ou.s systems. W. H.
Freeman. [AM]
(1983) Implications for neuroethology kom comparative neurophysiology.
In: Adwnces in wrtebrate nertroethology. ed. J. -P. Ewcrt, R. R.
Capranica & D. J. Ingle. Plenum Press. [J-PE]
(1983) Neurohiological roots and neuroethological sprouts. In:
Nettroethology and behacwral physiology, ed. F. Huber & H. Markl.
Springer-Verlag. [THB]
Burrows. M. (1980) The control of sets of motoneurones by local
interneurones in the locust. Journal of Physwbgy 298:213-23. [CHFR]
Burrows, M. & Hoyle, G. (1973) Neural mechanisms underlying hehavior in
the locust Schistocerca gregaria. 3. Topography of limb motor neurons in
the metathoracic ganglion. ]ourno1 of Neurobiology 4:167-86. [taGH]
Camhi, J. M. (1984) Neuroethology. Sinauer. [tarCH]
Carefoot. T. H. (1967) Growth and nutrition of three species of opisthobranch
molluscs. Cornparatice Biochei~tistyand Physiology 21:627-52. [IK]
Carew. T. J.. Abrams. T. W.. Hawkins. R. D. & Kandel, E. R. (1983) A test
at identificd synapses which mediate classical
of Hehb's post~~late
conditioning in Aplysia. Netrroscieitce Abstracts 9(1):168. [RDF]
Carew. T. J., Hawkins, R. D. & Kandel. E. R. (1983) Differential classical
conditioning of a dcfcnsive withdrawal rcflcx it1 Aplysia calfintica.
Science 219397-400. [SG]
Carlson, J. (1977) Tlie irnagitral ecdysis of the cricket (TeleOgn~/ltrsoceanicrrs).
I. Organization of motor programs and roles of central and sensory
control. 2. The roles of idcntifietl motor units. j o u n ~ a olf Coinparatiw
Ph!l.~iology115: 299-318, 319-336. [CHFR]
Carpenter. G. A. & Grossberg, S. (1981) Adaptation and transmitter gating in
vertebrate photorcceptors. jorrntal of Theoretical Netrrobiology 1:I42. [SG]
(1983a) Dynamic modcls of ncural systems: Propagated signals,
photoreceptor transduction, and circadian rhythms. In: Oscillations in
matheinatical biology, ed. J. P. E. Hodgson. Springer-Verlag. [SC]
(1983b) A neural theory of circadian rhythms: The gated pacemaker.
Biological Cybernetics 48:35-59. [SG]
(1984a) A neural theory of circadian rhythms: ~ s c h o f f srule in diurnal and
nocturnal mammals. Ainerican jorrrnal of Physiology. In press. [SG]
( 1 W b ) A neural theory of circadian rhythms: Split rhythms and long-term
after-effects. Submitted for publication. [SG]
Cattacrt, D. & Clarac, F. (1983) Influence of walking 011 swimmeret beating
in the lobster Hoinarus garninarus. ]ourno1 of Neurobiology 14:42139. [FC]
Coghill, G. E. (1929) Anatomy and the problem of behaciour. Cambridge
University Press. [taGH]
Cohen, J. L., Weiss, K. R. & Kupfermann, 1. (1978)]011ml of
Neurophysiology 41:157-80. [IK]
Cotnrm, J. H., Jr. (1977) Retrospectroscope: Insights into medical discowry.
Von Gehr Press. [THB]
Comroe, J. H., Jr., & Dripps. R. D. (1976) Scientific basis for the support of
biomedical science. Science 192:105-11. [THB]
Craig, W. (1918) Appetites and aversions as constituents of instincts.
Biological Bulletin 3491-107 [taGH]
Creuzfeldt, 0.D., Abbott, B. C., Fowler, W. M. & Pearson, C. M. (1963)
Muscle rnembranc potentials in episodic ad~namia.Electroencephabgraphy and Clinical Neurophysiology 15:508-19. [taCH]
Croll. R. P. & Chase, R. (1977) A long-term memory for food odors in the
land snail, Achatina firllica. Behacioral Biology 19:261-68. [ E m ]
Davis, W. J. (1968) Quantitative analysis of swimmeret h a t i n g in the lobster.
journal of Experimental Biology 48:643-62. [FC]
Delcomyn, F. (1980) Neural basis of rhythmic behavior in animals. Science
210:492-98. [taGH]
Deutsch. J. A. (1960) The strtrctural basis of behavior. Cambridge University
Press. [DLM]
Dewsbury, D. A. (1978) What is (was?) the "fixed action pattern"? Aniinal
Behaoiour 26:310-11. [DLM]
Dismukes, R. K. (1979) New concepts of molecular communication among
neurons. Behacioral and Brain Sciences 2:409-48. [taCH]
Dorsett. D. A.. Willows, A. 0. D. & Hoyle, G. (1973) lPle neuronal basis of
behavior in Tritonia. 4. The central origin of a fixed action pattern
demonstrated in the isolated brain. ]oun~al of Netrrobiology 4:287300. ItaCH]
Drummond. H. (1981) The nature and description of behavior patterns. In:
Perspecticas in ethology, ed. P. P. G. Bateson & P. H. Klopfer, vnl. 4.
Plenum. [WMS]
Ellis. P. E. & Hoyle, G. (1954) A physiological interpretation of the marching
of hoppers of the ~ f r i c a nmigratory locust (Locusta tnigratoria migratorioides R. and F.). ]ournal of Experimental Biology 31:271-79. [taGH]
Elsner, N. & Popov, A. V. (1978) Neuroethology of acoustic communication.
Adwnces in Insect Physiology 13:229-355. [tarGH]
Erber, J. (1983) Search for neural correlates of learning in bees. In:
Behaeioral physiology and neuroethology: Roots a n d growing points, ed.
F. Huber & H. Markl. Springer-Verlag. [GE.taGH]
Evarts. E. V. (1976) Neuronal representation of acquired movement patterns
in primates. In: Simpler neruous networks, ed. J. C. Fentress.
Sinauer. [DMC]
Ewert, J -P.(1980) Neuroethology, trans. Transemantics, Inc. SpringerVerlag. [MAA SG, taCH]
(1984) Concepts in vertebrate neuroethology. In: Aniinal behaciour. In
press. [J-PE]
Ewert, J -P., Capranica, R. R. & Ingle. D. J., eds. (1963) Adoances in
wrtebrate nerrroethology. Plenum. [GE, DMG. tarCH, DJI]
Ewing, A. & Hoyle. C. (1965) Neuronal mechanisms underlying cuntrol of
sound production in a cricket: Achcta domesticus. ]ourno1 of
Experii~untalBiology 43139-53. [rGH]
Ewing. A. & Manning, A. (1966) Some aspects of the effercnt cnntrol of
walking in three cockroach species. ]oumal of Insect Physiology 12:111518. [taCH]
Fentress. J. C. (1980) How can hehavior be studied from a neuroethological
perspective? In: l n f o m t i o n processing in the ilercous systern. ed.
Harold M. Pinsker & William D. Willis. Jr. Raven Prcss. [taCH]
(1981)Sensorimotor dcvclopmcnt. In: Dewlupinent of perception, ed. R.
N. Aslin. J. R. Albcrts & M. R. Petcrscn. Academic Prcss. [rGH]
Fernald, R. D. (1983) Neural basis of visual pattern recognition in fish. In;
Adwitces in vertebrate neuroethology, ed. J-P. Ewert. R. R. Capranica &
D. J. Itigle. Plenum. [taGH]
(1984) Vision and behavior in African cichlid fish. American Scientist 72;,%65. [HDF]
Finely, J., Ireton, D.. Schleidt, W. M. & Thompson, T. A. (1983) A new look
at the features of mallanl coltrtship displays. Animal Behaoiour 3134854. [WMS]
ReferenceslHoyle: Neuroethology
Flynn. j. (1972) Patterning mechanisms, patterned reflexes, and attack
behavior in cats. Nelrrasko Syrn~)osiunlon Motitiation 20:125-54. lDJll
Flynn, J. P., Vanegas. H., Foote, W. & Edwards, S. (1970) N e ~ ~ r a l
mechanisms involved in a cat's attack on a rat. 111:The neural control of
behatiior, ed. R. E. Whalen, H. F. Thon~pson,M. Verreano & N. M.
Weinherger. Academic Press. [HDSJ
Forman, R. (1982) A new paradigm permits the analysis of neurnnal
mechanisms underlying learned leg position in i:lsects. Doctoral
dissertation. University of Oregon. [taGH]
Frisch, K. von (1967) The dunce lar~grragerind orientation r,f bees. Harvard
University Press. [taGHj
Gallistel, C. R. (1'380) The organktion of action: A new synthesis. Erlbaum
Associatcs. [taGH]
Gandelnian. R. (1983) Gonadal hormones and sensory tinction.
and Biobehacioral Recieus 7:I -17. [HDS]
Getting, P. A. (1976) Afferent neurons mediating escape swimming of the
marine mollusc, Tritonia. ]oerrw[ of Cornparatice Physiology 110:27186. [CHFR]
(1983) Mechanisms of pattern generation t~nderlyingswimming in Tritonia.
3. Intrinsic and synaptic mechanisms Lrr delayed excitation. ]otrn~olof
Neurophysiology 4931036-50. [taGH]
Goodman, <:. S. & Spitzer, N. ( 2 . (1979) Embryonic devclopmr-nt of
identified neurons: Differentiation from ner~roblastto neurnne. Natrrre
280:208-14. [taGH]
Cottlieb, G., ed. (1973) Behatiioral ernbyology. Academic Press. [HDS]
4, (1976) Neural and behatiioral spec$city. Academic Press. [HDS]
Gray, J. (1950) The role of peripheral sense organs during locomotion in the
4:112vertebrates. Symposia of the Society for E ~ p r i n l e n t a Biology
26. [taGH]
Grillner. S. (1981) Control of locomotion in bipeds, t e t r a d s and fish. In:
Ifandhook of physiology, sect. 1. vol. I1 Motor control. ed. V. B. Brooks.
American Physiological Society. [FC]
Crosslxrg. S. (1968) Some physiological and biochemical consequences of
psychological postulates. Proceedings of the National Academy of Sciences
60:758-65. [SG]
(1969a) On the production and release of chemical trans~nittcrsand related
topics in cellular mntrol. Journal of Theoretical Biology 2232564. [SG]
(19691))Some networks that can learn, remember, and reproduce any
number of complicated space-time patterns. I. jorrrnal of Mathenlatics
and Mechanic.$ 19:53-91. [SG]
(1971) On the dynamics of operant conditioning. lorcrnal of Theoretical
Biology 33: 225-55. [SGI
(1972) A neural theory of punisl~mentand avnitlancc. 2. Quantitative
15:253-G. [SG]
theory. M a t h a ~ t i c o Biosciences
(1975) A neural model of attention, reinforcement, and discrimination
learning. Intenrationu1 Reciew ~.ofNetirobiology183263-327. [SGJ
(198%) Studies of mind and brain: Nerrrol principles of learning.
perception, dewlop~nent.cognition, and rnotor control. Reidel
Press. [SG]
(1982b) Processing of expected and unexpected events t l u r i ~ ~c~)nditioning
and attention: A psychophysiological theory. Psychological Rmiew
89:529-72. [SG]
(198%) A psychophysiological theory of reinforcement, drive, motivation,
1286-369. [SG]
and atten tion. ]orrrnal of Thmreticul Ne?etrro~)iu~ogy
(1983a) Some psychophysiological and pharmamlogical correlatrs of a
developmental, cognitive. and motivational theory. In: Brain and
infonmtion: Even! rebted potentials cd. H. Karrcr. J. Cohen & P.
Tucting. New York p cad em^ of Sciences. [SG]
Grossherg. S. & Kuperstein, M. (1984) Adaptive neural dynamics of the
sarudic eye movemcnt system and general principles of sensory-motor
rnntrol. Sobmittetl for publication. [SG]
Guthrie, 1). M. (1980) Neuroethology. Blackwell. [taGH]
Hampson. S. & Kil)ler, D. (1983) A Boolean complete ne~rralmotlel of
adaptive behavior. Biological Cybernetics 493-19. [rCHJ
Hassenstcin, B. (1983) F~~nktio~lssclialtl)ilcler
als Hilfsnlittel zur Darstellt~ng
theorctischer Konzepte in der Verhaltensbiologic. Zoolugische
lahrbiicher-Abteiltrng Physiologie 87: 181-87. I WMSJ
Hawkins. R. D., Abrams. T. W.. Carew. T. J. & Kandel. E. R. (1&3) A
cellular mechanism of classical ru)nditioning in Aplysia: Activitydependent a~nplificationof presynaptic facilitation. Science 219:4005 [SG ETW]
Hebb, D. 0. (1949) The organitatior~of behutiior. Wiley. (Science Etlitions
reprint, 1961). [JAS]
Heiligenhcrg, W. F. (1982) The jamming avoidance respnnse in an electric
fish. In: Adwncea in tiertebrate trerrruethology. ed. J. -P. Ewert. R.
Capranica. & D. J . Ingle. P l c n ~ ~ m [DJII
Heitler, W. J . (1974) The Iczt~stjump. Specialization of the mctathoracic
fcmorcr-tibia1 joint. jo~rrnulof Cos~paratiwPhy.s~ology89:93104. [taCH]
Hinde, R. A. (1970) Anirnal behaciur: A synthesis of ethology and cornpurcrtice
psychology. 21rtl ed. McGraw-Hill. [PB, ETW]
(1982) Etho/og!y: Its nattcrc and relnfions with other rcicnce.s, Oxhtrtl
University Press. IRDF. DLM]
Hinton. G . E. & Anderson. J. A., eds. (1981) Parallel rnodels of associatiw
~nernory.Erlbaum Asscwiates. [MAA]
Holst. E. v. (1939) L)ic relative Koortlinatio~~
als Pltacr~olnen11ntl als Methocle
zentralnewoeser Funktionsanalyse. Ergelrnisse der Physiologie 42228306. [WMSJ
Hoy, R. R. & Paul, R. C. (1973) Genetic control of song specificity in
crickets. Science 180:82-83. [taCH]
Hoyle, G. (1953) "Slow" and "fast" nerve fibres in lwasts. Natrrre
172:165. [taGH]
(1954) Changes in the blood potassium concrntration of tlre African
mipatory locr~st(L~custa~nigratoriamigraforioides R. and F.) during
food deprivation, and the effect on neuromuscular activity. Jorirol of
Experimental Biology 31:260-70. [taC;HI
(1957) Nervorls control of insect mr~scles.In: Hecent adwnces in
intier~ebratephysiology, ed. B. T. Scheer. University of Oregon
Press. [rGHl
(1964) Exploration of nerlronal mechanisms u~~derlying
L~haviorin insects.
In: Netrral theon] and modeling, ed. R. F. Reiss. Stanford University
Press. [tarGH, AM1
(1965) N e ~ ~ r o ~ h ~ s i o l o gstudics
i c a l on "learning" in headless insects. 111:
Physiology of the insect central nerwus system, ed. J. W. Bea~nent& 1.
Treherne. Academic Press. [rGH]
(1967) Specificity of muscle. In: Inwrtebrate nerwus systerns, ed. C. A. C.
Wiersma. University of Chicaw) Press. IDLMJ
(1970) Cellular mechanisms underlying behavior - Neuroethology.
Adconces in Insect Physiology 7349-444. [FD. J-PE, taGH]
(1974) A function for neurons (DUM) neurosecretory on skeletal musclc of
insects. Jo~irnalof Eq~eriirrentalZar,logy 189:401-6. ItaGH]
(1975) ~dentifiedneurons and the future of n e ~ ~ t h o l o glourno1
Experinlental Zoology 19451-74. [FC, FD, taGHj
(1976) Approaches to understanding the neurophysiological bases of
behavior. In: Simpler networks and hehatiiur, cd. J. Fentress.
Sinauer. [FC, taGH, IK. DLM, AM]
(1977) Kees Wiersma: An appreciation. In: Identified neurons and lrehacior
of arthropods. ed. G. Hoyle. Plcnum. [JPE. DLM]
(1980) Learning, ([sing natural reinforcements, in insect preparations that
permit cellular neuronal analysis. lournal of Nerrrobiology 11:32354. [FC, laGH]
(1983) Forms of mod~~latable
tension in skeletal muscles. Cornparatice
Biochemistry and Physiology 76A:203-10. [taCH]
(1984) Neuromuscular transmission in a primitive insect: Modulation by
octopamine, ant1 catch-like tension. Comparatitx Biochemistry and
Physiology 77c:219-32. [rGH)
ed., (1977) Identifed neurons a n d behavior of arthropods. Plenum. IFC]
ed., (1977) IdentiJ~d neurons and behacior of arthropods, preface.
Plenum. [J-PE]
Huhel. D. H. & Wiesel, T. N. (1974) Sequence regularity and geometry of
orientation cnlumns in the monkey striate cortex. ]otrrnal of Contparutifie
Nerrrolo~y158:267-94. [CHFRJ
Hulrer, F. (1983) l~nplicationsof insect ~~eurocthology
for studics on
vertebrates. In: Adtiances in certebrate nerrroethology, ed. J. P. Ewert,
R. H. Capranica & D. J. Ingle. Plenum. [GE]
(1983) Neural r~)rrelatesof orthopteran and cicada phonotaxis. In:
Neuroetholugy and hehacioral physiology, cd. F. H u h & H. Markl.
Springer-Verlag. [JE]
Huber, F. & Markl. H., eds. (1983) Behatiioral 1)hysiologyand neeroethology:
Roots and grottiing points. Springer-Verlag [GE]
Hughes. T. D. (1980) The imaginal edysis of the desert locust. Schistocerca
gregaria. 1. A description of the behaviour. 2. Motor activity underlying
the pre-emergence and emergence behavioi~r.3. Motor activity
underlying the expansional and post-expnsional behaviour. 4. The role of
the gut. Physiological Entonwlogy 547-54, 55-71. 141-52. 15364. [CHFH]
Inselman-Temkin, B. R. & Flynn, J. P. (1973) Sex-dependent effects of
gonadal and gonadotropic hormones on centrally elicited attack in cats.
Brain Research 60:393-410. [HDS]
facklett. J. W. (1969) Circadian rhythm of optic nerve impulses recorded in
darkncss from isolated eye of Aplysia. Scierice. 164:562-63. [SG]
Jahanpa~war.B. (1972) Behavioral and electrophysiolngical studies on
chemoreception in Aplysia. American Zwlogist 12:529-37. [IK]
Kandel. E. (1976) The cellrrlar basis of behatiior. Freeman. [JD, taGH, JZYj
(1979) Behacioral biology of Aplysia. Freeman. [MAA. J D , taCH, AM.
ReferenceslHoyle: Neuroethology
ande el, E. & Schwartz. J . H. (1982) Molcc~rlarbiology of learning:
Moclulation of transmitter release. Science 218:433-42. [JD, taCH]
Kennedy, J. S. (1954) Is modern ethology ol)jcctive? British Jotrr~ralof Airiina/
Behatiinur 2:12-19. [taGH]
Klopf. H. (1982) The hedonistic neuron. Hemisphere. [rC.H]
Konishi, M. (1983) Localization of acciustic signals in the owl. In: Admtices in
tiedebrate r~errroethology,ed. J.-P. Ewert, R. R. Capranica & D. 1.
Ingle, Plenum. [taGH]
Kriegstein, A. R. (1977) Drvelopment of the nervous system of Aplysia
califurnica. Proceedings of the Notional Acodeii~yof Sciences 7437578. [ETW]
Kupfermann, I. (1974) Feeding behavior in Aplysia: A simple system for the
study of motivation. Behocioral Biology 10:l-26, Abstract No.
3169. [IK]
Kupfcrmann, 1.. Cohen, J. L., Mandelbau~n,D. E., Schonberg, M.,
Susswein, A. J. & Weiss, K. R. (1979) Functional role of serotonergic
neuromodulation in Aplysia. Federation Proceedings, Ai~~crican
Society of
Experimental Biology 3H:2095-102. (FC]
Kupfermann, I. & Weiss, K. (1978) The command neuron concept.
13-39. [J-PE. taGH]
Behatiioral and Brain Scie~~ces
Lara, R. & Arbib, M. A,, eds. (1983) Proceedings of the second wrkshop oil
tiisrroiwtor coordinotioi~ill jiog and toad: Models and erp~riments.
Technical Report 83-19, Department of Computer and Information
Science. University of Massachusetts at Amherst. [MAA]
Lashley, K. S. (1929) Broin mechanisins and intelligence. University of
Chicago Press. (Dover reprint, 1963). [JAS]
Lewis, W. E., Mishkin, M., Bragin, E., Brown, R. M.. Pert. C. B. & Pert,
A. (1981) Opiate receptor gradients in monkey cerebral cortex: Correspondence with sensory prooessing hierarchies. Scieilce 211:1166-69. [HDS]
Lennard, P. R., Getting. P. A. & Hume, R. 1. (1980) Central pattern
generator mediating swimming in Tritonia. 2. Initiation, maintenance,
and termination. ]orrrnul of Neuruphysiology 44:165-73. [CHFRJ
Lindkrg, D. & Elsner. N. (1977) S e ~ ~ s o rinfluence
opou grasshopper
stridulation. Natrrnoissenschaften 64342. [taCHj
Leonard, J. L.. & Lukowiak, K. (1982) An ethological analysis of mating in
Nawnax inennis (Mollusca: Opisthobranchia). Society for Neuroscience
Abstro~cts8:607. [ILL]
(1983) The behavior of Aplysia colifornica: Ethogram and ethological
analysis of mating. Society for Neuroscience Abstracts 9:534. [JLL]
(in press a) An ethogram of the sea slug Natiunx ir~ennis(Opisthobranchia.
Gastropoda). Zeitschrift fiir Tierpsychologie. [JLL]
(in press b) Male-female conflict in a simultaneous hermaphrodite resolved
by sperm trading. Arnerican Natrrralist. [JLL]
h r e n z , K. Z. (1931) Beitrage zur Ethologie sozialer Corciden. journal of
Ornithology 75:511-19. [taGH]
Lorenz, K. (1932) Betraclrtungen iiber das Erkennen der arteigenen
Triebhandlungen bei Vocgeln.]wrnalfiir Ornithologie 80:N-98. [WMS]
(1936) ~ b e die
r eigentiimliche Velliind~~ng
branchialer Hirnnerven hei
Cypselus opw. Moryhologisch~sjahrbuch 77:305-25. [WMS]
(1937) Uber die Bildung des Instinktbegriffes. Nat~rru;issenschaftei~25:298300, 324-31. [WMS]
(1943) Die angeborenen Formen moeglicher Erfahnrng. Zeitschrift fijr
Tierpsychologie 5:235-409. [WMS]
(1950) The cmnparativc method in stutlyirlg innatc behavior patterns.
Symposia of the Societyfor E z p e r i n ~ n t aBiology
4:221-68. [taCH,
(1958) The evolution of behavior. Sciei~tificAmerican 199:67-78. [ E n q
(1965) Etiolution and inodificatbi~of 1,~hociur.University of Chicago
Press. [PB, WMS, ETW]
(1970) Studies in anirnul and hrrn~anbehatiior, vol. 1. Harvard University
Press. [WMS]
(1981) The forrnhtions of ethology. Springer-Verlag. [GE. J E , HAH,
Lynch, J. C. (1980) The functional organization of posterior parietal association
cortex. Behatiioral and Broin Sciences 3(4):485-534. [HDS]
McAllister. L. B., Scheller, R. H., Kandel, E. R., & Axel. R. (1983) In situ
hybridization to study the origin and fate of identified neorons. Science
222:800-8. [ETWJ
McClosky, D. 1.. Colebatch, J. C., Potter, E. K. br Burke, D. (1983)
Judgements ahout onset of rapid voluntary movements in man. ]orrrnol of
Neurophyswlogy 48:851-63. [RDF]
McCulloch, W. S. & Pitts, W. H. (1943) A logird calculus of the ideas
immanent in nervous activity. Bulletin of Mothernutical Biophysics 5:11533. [MAA, taGHJ
McDougall. W. (1923) An Outliiie of Psychology. Methuen. [taCH]
MacKay, W. A. (1980) The motor programs: Back to the c o ~ n p ~ ~ Treitds
t r r . in
Neurosciences 397-100. [FC]
Manning, A. (1972) An introduction to aniinol behotiiour. 2nd ed.
Arnold. [DMG. taGH. ETWj
(1979) An introd~rctionto rii~iomlbehacio~rr,3rd t ~ l .Arnsrld. IDLM]
Markowitsch. H. J. & Pritzel, M. (1978) Siugle unit i~ctivityill cat prefrontal
artd posterior associatio~~
cortex (luring pel.forn~;~ncc
of spat131rcscarcl~
tasks. Broin Rescorch 149:53-75. IDMGJ
Marr. D. (1982) Vision: A corn~)rrtotioi~nl
ii~tiestigotwrrillto the h~rirmn
represet~tationond proce.wing ofcisrrol ir$onnation. Freemall. (MAA,
Marr, 1). & Poggio, T. (1977) From understanding cornputation to
understanding neural circuitry. Nerrmscier~cesReseorch Prc~grcrii~
15:470-88. [MAA]
Marzio, P. C. (1973) Rube Coldberg - Iiis life and w r k . Harper &
Row. [WMS]
Medawar, P. (1967) The art of the sol~rble.Meth~ren. [DLM]
Merton, P. A. (1953) Spinal reflex action. 111:The spir~alcord. Ciba
Symposium. Churchill, London,l-24. [DMG]
Mesulam, M. M., M~rfson.E. J., Levey. A. I. & Wainer. B. H. (1983)
Cholinergic innervation of cortex by the basal brebrain: Cytc~hemistry
and cortical connections of the scptal area, diagonal band nuclei, ~ ~ u c l c ~ ~ s
basalis (substantia innominata), and hypothalarnos in the rhcsus monkey.
lotrrnal of Coinparatitie Ne~rrology214:170-97. [HDS]
Minsky. M. & Papert, S. (1969) Perceptions: An ii~trodrrctionto cornprrtolional
gemnety. MIT Press. [rCHj
Morasso. P. (1981) Spatial control of arm movements. Ezperi~ilei~tal
Research 42:223-27. [rGH]
Morris, D. (1967) The nuked ope. McGraw-Hill. [baGH]
Nevatia. R. (1982) Machine perception. Prenticc-Hall. [MAA]
Nottebohm, F., Stokes. T. M. & Leonard, C. M. (1976) Central control of
song in the canary. journal of Coniparotiw Nerrrolugy 16545786. [taGH]
Nyquist. H. (1932). Regeneration theory. Bell Systen~sTechnical]ournol.
lI:126-47. [DMG]
Ohta, M. (1982) Work reviewed in T. 0 . Binford, Survcy of model-based
image analysis systems. lnternotionol journal of Robotics
Research. [DMG]
O'Shea, M. & Williams, J. L. D. (1974) The anatomy and output connection
of a locust visual interneurone: The lohular giant movement detector
(LGMD) neurone. Journol of Cot~~paratitie
Physiology 91:257-66.
Ostriker, G., Pellionisn. A. & Llinas. R. (1982) T e ~ ~ s uetwork
thcory applied
to the otulomotor system: CNS activity expressed with natrrral. nonorthogonal coordinates. Abstract No. 45.2, 12th Annual Meeting of the
Society for Ne~rroscience,Mi~~neapolis.[taCHJ
Paillard, J. (1960) The patterning of skilled movement. In: Handbook of
physiology, Sect. 1, vol. 111 Nerrrophysiology, ed. J. Fields. H. W.
Magoun. & W. E. Hall. American Physiolo~icalSociety. [FC]
(1983) Introductory Iccture: The fi~nctionallaliellil~gof neural codes. In:
Neurol coding of inutor performance, Experiiner~tolBrain Reseroch Sop.
7, ed. J. Massion. J. Paillard. W. Schultz & M. Wiesendangey. SpringerVerlag. JFC]
Passmore, J. (1970) The perfectability of mun. New York. [taGH]
Puarsoo. K. G. (1976) Nerve cells w i t h o ~ ~
potentials. In: Siiiq~ler
networks ond behatiior, ed. J . C. Fentress. Sinauer. [taGHl
Pearson, K. C. Heitler. W. J. & Steeves, J. I). (190) Triggering of locust
jump by multimodal inhibitory interneurons. ]otrri~alof Nerrrophysiology
43957-78. [taCH]
Pearson. K. G. & Robertson. R. M. (1981) l n t e r ~ ~ e u r ocoactivating
flexor aud extensor motoneurous in the lncrrst. ]vrirr~ol of Cmnparatitie
Physiology A 144:391-400. [taCH]
Pellionisz, A. & Llina. R. (1979) Brain modelling by tensor network theory
and computer simulation. The cerebellum: Distributed processor for
predictive ctwrdination. Netrrascience 4:323-48. [rGH]
Perachio, A. A. (1978) Hypothala~nicregulation of behavioral and hormonal
aspects of aggression and sexual perforn~ance.In: Recent adtiances in
priinatology. vol 1, Behatiior, ed. D. J. Chivers & J. Herbert. Academic
Press. [HDS]
Perret, C., Millancvoye, M.. Cabelguen, J. M. (1972) Messages spinaux
ascendants pendant une I(xvmotion fictive chez le chat curanis&. ]ourno/
de Physiologie 65:153. [FC]
Peterson, E . L. (1983a) Generation and coordination of heartbeat tirning
oscillation in the medicinal leech. 1. Oscillation in isolated ganglia.
lourno1 of Ne~rrophysiulogy49:611-26. [taCH]
(1983b) Generation and coordination of heartbeat timing oscillation in the
medicinal leech. 2. Intersegmental coordination. Jotrrnal of
Netrrophysiology 49:627-38. [taCHj
Pfaff, D. W. (1980) Estrogens ond broinfrinctiun. Springer-Vcrlag. [HDS]
Pf&> D. W., Lewis, C., Diakow, C. & Keincr, M. (1973) Ne~~rophysiological
analyses of mating behavior responses as hormone-sensitive reflexes. In:
Progress in physiological psychology, ed. E. Stellar & J. M. Spragoe.
Academic Press. [DJI]
41 1
ReferenceslHoyle: Neuroethology
Pinsker. H.. Herring, W. A.. Carew, T. J. & Kandcl, E. R. (1973) Long-term
sensitization of a defensive withdrawal reflex in Aplysia. Science
182:1039-42. [ETW]
Prechtl, H. F. R. (1956) Ne~roph~siologische
Mechanismen des Formstarren
Verhaltens. Behavior 9:246-319. [AM]
Preston, R. J. & Lee. R. M. (1973) Feeding behavior in Aplysia californico:
Role of chemical and tactile stimuli. jo~rrnalof Coinparatitie and
Physiological Psychology 82:368-81. [IK]
Pringle, J. W. S. (1939) The motor mechanism of the insect leg. J o ~ r n ~of
Experimental Biology 16:220-31. [taCH]
Rehbein. H. (1976) Auditory neurons in the ventral cord of the locust:
Morphological and functional properties. Journal of Comparatice
Physiology A 110:233-50. [taCH]
Reichardt, W. & Poggio. T. (1976) Visual control of orientation behavior in
the fly. I.: A quantitative analysis. Quarterly Retiieuts of Biophysics
9:311-75. [MAA]
Reichardt, W., Poggio. T. & Hansen. K. (1983) Figure-ground discrimination
by relative movement in the visual system of the fly. Part 11: Towards the
neural circuitry. Biological Cybernetics. 46(Suppl. 1):l-30. [rGH]
Reichert, H. (in press) The cellular basis of sensorimotor coordination in the
flight control system of the locust Locusta migratoria. In: Bilateral and
interseginento1 coordimtion, ed. B. M. H. Bush & F. Clarac. Cambridge
University Press. [CHFR]
Roeder. K. D. (1967) N e m cells and insect behatiwr. Harvard University
Press. [FD, taGH]
(1975) Neural factors and excitability in insect behavior. Journal of
Experimental Zoology 194:75-88. [taCH]
Reiss, R. F., ed. (1964) Neural theoy and modelling. Stanfoid University
Press. [rGH]
Rose. J. D. & Michael. R. P. (1978) Facilitation by estradiol of midbrain and
pontine unit responses to vaginal and somatosensory stimulation in the
squirrel monkey (Saimiri sciureus). Experimental Neurology 58:4658. [HDS]
Rothenbuhler, W. C. (1964a) Behaviour genetics of nest cleaning in honeybees. 1. Responses of four inbred lines to disease-killed brood. Animol
Behatiiour 12:578-83. [taGH]
(1964b) Behaviour genetics of nest cleaning in honey-bees. 4. Responses of
F and backcross generations to disease-killed brood. Ainerican
4:111-23. [taCH]
Rowell, C. H. F. (1971) The orthopteran descending movement detectors
(DMD) neorones: A characterisation and review. Zeirschrififiir
Vergleichende Physwlogie 73:167-94. [taCH]
Rowell, C. H. F., O'Shea, M. & Williams, J. L. D. (1977) The neuronal basis
of a sensory analyser, the acridid movement detector system. 4. The
preference for small field stimuli. Journal of Experimental Biology
68:157-85. [CHFR]
Russell, E. S. (1934) The behatiiour of a n i d . Arnold. [taCH]
Sackett, G. P. (1966) Monkeys reared in isolation with pictures as visual
input: Evidence for an innate releasing mechanism. Science 154:146873. [HDS]
Sahley, C., Rudy, J. W. & Gelperin, A. (1981) An analysis of associative
learning in a terrestrial mollusc. 1. Higher-order conditioning, blocking,
and a transient US pre-exposure effect. Journal of Comparatice
Physiology A 144:l-8. [ETW]
Satou, M. & Ewert, J. -P. (1984) Specification of tecto-motor outflow in toads
by antidromic stimulation of tecto-bulbjarlspinal pathways.
Natumissenschaften 7152-53. [J-PE]
Scheich, H. (1983) Sensorimotor interfacing. In: A d c a m in wrtebrate neumethology, ed. J. P. Ewert, R. R. Capranica & D. J. Ingle. Plenum. [Gel
Scheller, R. H., Rothman. B. S. & Mayeri, E. (1983) A single gene e n d e s
multiple peptide-transmitter candidates involved in a stereotyped
behavior. Trendr in Neurosciences:340-45. [RDF, CHFR]
Schleidt, W. (1962) Die historische Entwicklung der Begriffe "Angelmrencs
auslosendes Schema" und "Angeborener Auslnsemechanismus" in der
Ethologie. Zeitschrift f i r Tierpsychologie 19:697-722. [J-PE]
Schleidt. W. M. (1964) Uher die Spontaneitaet von Erl~koordinationcn.
Zeitschrift fiir Tierpsychologie 21:235-56. [WMS]
(1965) Gaussian interval distribution in spontaneously occurring innate
behavionr. Nature 206:1061-62. [WMS]
(1974) How "rued" is the Fixed Action Pattcra? Zeitschrift fir
Tierpsychologie 36:184-211. [taCH, WMS]
(1981) The behavior of organisms, as it is linked to genes and populations.
111: Perspectities in ethology, ed. P. P. G. Bateson & P. H. Klopfcr, vol.
4. Plennm. [WMS]
Schleidt, W. M. & Crawley, J. N. (1980) Patterns in the bel~aviourof
organisms. Jotrrnal of Social and Biological Structures 31-15. [WMS]
Schneidcr. G. E., Jhaveri. S., Edwards, M. L., & So, K. F. (1984)
Regeneration, ronting, and re-distribution ofaxons after early lesions:
Changes with age and fnnctional impact. In: Adwncrs in neurology. cd.
J. C. Eccles & M. A. Dimitrijevic. Raven Press. [DJII
Schneirla, T. C. (1952) A consideration of some conceptual trends in
comparative psychology. Psychological Btrlletin. 49:559-97. [taCHI
Selverston, A. 1. (1980) Are central pattern generators understandable?
Behaoioral and Brain Sciences 3:535-71. [FC. JD.taGH]
Selverston. A. I., Russell, D. F., Miller, J. P. & King, D. C. (1976) The
stomatogastric nervous system: Structure and function of a small ncu~;~l
network. Progress in Nerrrobwlogy 7:215-90. [JD, taCH]
Sherrington. C. S. (1906) The integratitle actwn of the n e m u s systein.
Scribner's. [taCH, AM]
Simmons. I. A. (1980) The processing of sonar echoes by bats. In: Aniirml
s o m r system, ed. R. -G. Busnel & J. E. Fish. Plenum. [taCH]
Sombati, S. (1983) Orchestrating behaviors: A central modulatory role of
octopamine in the locust. Abstract No. 24.11, 13th Annual Meeting of the
Society for Neuroscience. Boston. [taCH]
Stent, G. S. (1981) Cerebral hermeneutics. Journal of Social and Bwlogical
Structures 4:107-24. [MAA]
Susswein, A,, Weiss, K. R. & Kupfermann, 1. (1978) The effects of food
arousal on the latency of biting in Aplysia. jotrrnal of Cornparatitie
Physiology I23:31-41. [IK]
Szentagothai, J. & Arbib, M. A. (1975) Concepttml inodels of neural
organization. MIT Press. [MAA]
Taub, E. (1977) Movement in nonhuman primates deprived of somatosensory
feedback. In: Exercise a n d spori science ret;ieu;s, vol. 4, ed. J. F. Kengh.
Journal Publishing Affiliates. [HDS]
Thompson, K. J. (1982) The neural mechanism of oviposition digging in
grasshoppers. Doctoral dissertation. University of Oregon. [taGH]
Thorpe, W. H. (1979) The origins a n d rise of ethology. Praeger. [taGH]
Tinbergen, N. (1951) The study of instinct. Oxford University Press. [DMC.
Truman, J. W. (1979) Interaction between abdominal ganglia during the
performance of hormonally triggered behavioural programmes in moths.
journal of Experitnental Biology 82:239-54. [CHFR]
Truman, J. W., Mumby, S. M. & Welch, S. K. (1980) Involvement ofcyclic
GMP in the release of stereotyped behaviour patterns in moths by a
peptide hormone. Journal of Experimental Biology 201-12. [CHFR]
Walters, E. T. & Byrne, J. H. (1983a) Associative conditioning of single
sensory neurons suggests a cellular mechanism for learning. Science
219:405-8. (SG, ETW]
Weiss, K. R. Koch, U. T., Koester, J., Mandelbaum, D. E. & Kupfermann.
I. (1981) Neural and molecular mechanisms of food-induced arousal in
Aplysia calqornica. Advances in Physiological Sciences 23:305-44. [IK]
Weiss, P. (1941) Does sensory control play a constructive role in the
development of motor coordination? Sch~ueizerMedizinkche
Wochenschrift 71:591-95. [taCH]
(1950) Experimental analysis of co-ordination by the disarrangement of
central-peripheral relations. Symposia of the Society for Experitnental
Biology 4:92-111. [tarGH]
West, I. C. (1953) Semmechanisms. English Universities Press. [DMG]
Wetzel, M. C. & Howell, L. G. (1981) Properties and mechanisms of
locomotion. In: Handbook of behatiwral neurolrwlogy. vol. 5: Motor
coordination, eds. A. L. Towe & E. S. Luschei. Plenum. [FC]
Wheeler, W. M. (1902) "Natural history," "oecology." or "ethology." Science
15:971-76. [taGH]
Whihnan, Ch. 0.(1819) Animal Behatiior. 16th lecture. Biology Lectures.
Woods Hole Publications, Mass. [taCH]
Wiener, N. (1948) Cybernetics. MIT Press. [taGH]
Wiersma, C. A. G. (1947) Giant nerve fibre system of the crayfish. A
contribution of comparative physiology of the synapse. Journal of
Neurophysiology 10:23-38. [CHFR]
(1974) Behavior of neurons. In: The neurosciences: Third strrdy program,
ed. F. 0 . Schmitt. MIT Press. [J-PE]
Wike, E. L., ed. (1966) Sewndo y reinforcement. Harper and Row. [SG]
Willows, A. 0 . D.. Dorsett. D. A. & Hoyle, G. (1973) The neuronal basis of
behavior in Tritonia. 3. Neurnnal mechanisms of a fixed action pattern.
Journal of Neurobiology 4:255-85. [taGH]
Wilson, D. M. (1972) Genetic and sensory mechanisms for locomotion and
orientation in animals. Ainerican Scientist 69:358-65. [taGH]
Wine, J. J. & Krasne, F. B. (1982) The cellular organization of crayfish escapv
hehavior. In: The biology of crustacea, vol. 111. ed. H . Atwond & I>.
SandenJan. Academic Press. [CHFR]
Wocdy, C. D., Swartz. B. E. & Gruen, E. (1978) EHects of acetylcholine a1111
cyclic GMP on input resistance of cortical neurons in awake cats. Brair~
Research 1%:373-95. [ETW]
Zaretsky. M. (1982) Quantitative measurements of centrally arid rcti~~ally
generated sawadic suppression in a l u c ~ ~movement
detector ncurnne.
journal of Physiology-Londtin 32R:521-33. (RDFI

Documentos relacionados

Untitled - Incubadora de Sites da USP

Untitled - Incubadora de Sites da USP rigorous methods of making science. The first paper can be considered a milestone in the ethological research in Brazil and Latin America. The second, an introduction to the historical development ...

Leia mais